Biology of

Amphibians
 Biology of
Amphibians

William E. Duellman
Linda Trueb
Illustrated by Linda Trueb

The Johns Hopkins University Press

Baltimore and London
Copyright 1986 by William E. Duellman and Linda Trueb
Preface © 1994 The Johns Hopkins University Press
All rights reserved
Printed in the United States of America on acid-free paper

First published in 1986 by the McGraw-Hill Publishing Company.

Johns Hopkins Paperbacks edition, 1994
_

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The Johns Hopkins University Press

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Baltimore, Maryland 21218-4319
The Johns Hopkins Press Ltd., London

Library of Congress Cataloging-in-Publication Data will be found at the end of this book.
A catalog record for this book is available from the British Library.
 Contents

BIOGRAPHICAL NOTE ix

FOREWORD BY CHARLES M. BOGERT xi

PREFACE xv

PREFACE TO FIRST EDITION xix

Chapter 1 INTRODUCTION TO THE AMPHIBIA 1

The World of Amphibians 1
Historical Resume 2
Prospects for the Future 7
Part 1 LIFE HISTORY

Chapter 2 REPRODUCTIVE STRATEGIES 13

Reproductive Cycles 13
Reproductive Mode 21
Quantitative Aspects 28
Parental Care 38
Evolutíon of Reproductive Strategies 47
Chapter 3 COURTSHIP AND MATING 51
Location of Breeding Site 51
Secondary Sexual Characters 52
Courts'hip Behavior 60
Fertilization and Ovipositíon 71
Sexual Selection 80
Evolution of Matíng Systems 85
Contents
Chapter 4 VOCALIZATION 87
Anuran Communication System 88
Mechanisms of Sound Production and Reception 89
Kinds of Vocalizations and Their Functíons 97
Abiotíc Factors Affecting Vocalization 104
Interspecific Significance of Vocalization 105
Phylogenetic Implications of Vocalization 107
Chapter 5 EGGS AND DEVELOPMENT 109
Spermatozoa and Fertilizatíon 109
Egg Structure 111
Egg Development 116
Hatching and Birth 133
Development and Amphibian Diversity 139
Chapter 6 LARVAE 141
Morphology of Larvae 141
Adaptive Types of Larvae 156
Physiology and Ecology 162
Social Behavior 169
Evolutionary Significance of Larvae 171
Chapter 7 METAMORPHOSIS 173
Endocrine Control 173
Other Biochemical Changes 178
Morphological Changes 182
Neoteny 189
Ecological and Evolutionary Significance of Metamorphosis 192

Part 2 ECOLOGY

Chapter 8 RELATIONSHIPS WITH THE ENVIRONMENT 197

Water Economy 197
Temperature 210
Gas Exchange 217
Energy Metabolism and Energy Budgets 224
Ecological Synthesis 225
Chapter 9 FOOD AND FEEDING 229
Prey Selection 229
Location of Prey 231
Capture of Prey 232
Evolutíon of Prey-Capturing Mechanisms and Strategies 238
Chapter 10 ENEMIES AND DEFENSE 241
Diseases 241
Parasites 242
Predators 244
Antipredator Mechanisms 246
Evolutíon of Defense Mechanisms 259
Chapter 11 POPULATION BIOLOGY 261
Characteristics of Individuáis 261
Movements and Territoriality 265
Demography 267
Factors Regulatíng Populations 272
 Contents
Chapter 12 COMMUNITY ECOLOGY AND SPECIES DIVERSITY 275
Community Structure 275
Species Diversity 281
Evolutíon of Amphibian Communities 284
Part3 MORPHOLOGY

Chapter 13 MUSCULOSKELETAL SYSTEM 289

Skull and Hyobranchium 289
Axial System 324
Appendicular System 335
Integration of Functional Units 364
Chapter 14 INTEGUMENTARY, SENSORY, AND VISCERAL SYSTEMS 367
Integument 367
Sensory Receptor Systems 379
Nervous System 390
Circulatory and Respiratory Systems 397
Urogenital System 405
Digestíve System 408
Endocrine Glands 411
Evolutionary Considerations 414
Part4 EVOLUTION

Chapter 15 ORIGIN AND EARLY EVOLUTION 417

Nature of a Tetrapod 418
Primitive Tetrapods 419
Tetrapod Afflnities: Lungfishes or Lobe-Fins? 424
Diversity and Evolutíon of Early Tetrapods 435
Status of the Lissamphibia 437
Chapter 16 CYTOGENETIC, MOLECULAR, AND GENOMIC EVOLUTION 445
Cytogenetics 445
Molecular Evolution 453
Genomic Evolution 458

Chapter 17 PHYLOGENY 461

Caudata 461
Gymnophiona 466
Anura 468
Chapter 18 BIOGEOGRAPHY 477
Biogeographic Principies 477
Historical Setting 478
Lissamphibia 482
Caudata 482
Gymnophiona 485
Anura 485
Chapter 19 CLASSIFICATION 493

LITERATURE CITED 557

INDEX 613

vü
Dedícation

To our gradúate students—

past, present, and future
 Biographical Note

William E. Duellman has been associated since 1959 with the University of Kansas,
where he is now curator of the División of Herpetology in the Museum of Natural
History, and Professor in the Department of Systematics and Ecology. He teaches
gradúate courses in biogeography, repule biology, and amphibian biology (with
Linda Trueb). He maintains an active gradúate program in herpetology, and he
and his students use the extensive herpetological collectíons in the museum for
diverse research. His studies on the systematics, ecology, and reproductive biology
of amphibians have involved extensive field work in the United States, México,
Central and South America, as well as Australia and África. Born in Dayton, Ohio,
he studied zoology at the University of Michigan, where he received a doctor's
degree in 1956. He taught at Wayne State University before joining the University
of Kansas.

Dr. Duellman's writings include more than 200 contributions to national and
intematíonal joumals, symposia, and museum publicatíons. Major works are Hy/id
Frogs of Mídale America (Monogr. Mus. Nat. Hist. Univ. Kansas, 2 vols., 1970);

IX
Biographical Note
Liste der Rezenten Amphibien und Repulen: Hylidae, Centrolenidae, Pseudidae
(Das Tierreich, vol. 95, 1977); and The Biology of an Equatoríal Herpetofauna in
Amazonian Ecuador (Mise. Publ. Mus. Nat. Hist. Kansas, vol. 65, 1978). He edited
The South American Herpetofauna: Its Origin, Evolution and Dispersa/ (Monogr.
Mus. Nat. Hist. Univ. Kansas, vol. 7, 1979).

Linda Trueb teaches at the University of Kansas. Her courses include scientific
illustration, evolutionary morphology, and (with William E. Duellman) amphibian
biology. She also maintains an active gradúate program in the Department of
Systematics and Ecology and in the Museum of Natural History, where she and
her students are invesrigating diverse aspects of vertébrate morphology. She has
carried out extensive field work in Central and South America and also has worked
in África and Australia. In 1979 she was a visiting lecturer at the University of
Adelaide, Australia. Originally from Pomona, California, Linda Trueb did her
undergraduate work at the University of California, Berkeley, with emphasis on
vertébrate zoology. At the University of Kansas she undertook research on cranial
osteology of anurans for the Ph.D, which she received in 1968. She has contínued
investigations on amphibian morphology and systematics, especially of tropical
groups of anurans, and has expanded her research to include functíonal mor-
phology and the role of heterochrony in anuran osteology. Aside from her re-
search, she is a practicing scientific illustrator.

The author of about 36 major, refereed papers, Dr. Trueb has published in both
domestic and foreign symposium volumes and in a variety of national and inter-
national seriáis, including Miscellaneous Publications and Occasional Papers of the
University of Kansas, Contributions to Science of the Los Angeles County Museum
of Natural History, Copela, Herpetologica, Journal of Morphology, Journal of Zoology
(London), and South African Journal of Science.
 Foreword
by Charles M. Bogert

Perhaps the earliest amphibians made their debut in an área with a more rigorous
climate, but their initial diversification could well have occurred in tropical envi-
ronments. Climatic conditions similar to those of today in the rainforests and cloud
forests of the tropics presumably prevailed during the Pennsylvanian Period when
amphibians were already numerous. For well over 250 million years amphibians
have been exploiting habitáis in moist tropical environments, where the bulk of
them remain. Either most living amphibians are restricted to such environments or
they belong to groups of species that have representatives with ranges extending
into the tropics. In fact, the Gymnophiona, the smallest of the three orders and
the one to which the only extant limbless amphibians are assigned, are known
solely from moist tropical environments. These superficially wormlike amphibians,
known as caecilians, include species that retain fishlike scales hidden in the skin.
Fossil caecilians, unknown untíl recently, shed little light on their ancestry, perhaps
the oldest of any amphibians extant.

Salamanders, the tailed amphibians grouped in the order Caudata, though rep-
resented in the American tropics, have the distinction of being more diversified in
the United States than elsewhere. Relatívely thorough investigations still in progress
in this country have already revealed 115 species, almost one-third of the total
now recognized. Salamanders continué to be discovered in México, which may
prove to support as many species as the United States. However, only 43 species
are known from Europe, a thoroughly explored continent.

The third order, the Anura, the most widely represented of any group of am-
phibians now living, contains the tailless species known as frogs and toads. These
include neary 87 percent of all amphibian species extant. During their long history

XI
Foreword
they have probably exploited all but the most inhospitable environments between
the poles and the Equator. Scarcely 3 percent of the species are represented in
the United States. Some of these are largely tropical, with distributions that extend
northward to the southem típ of Texas.

Although only one popular account of amphibians, The Frog Book (1906), was
available until around 1940, a wealth of authoritative handbooks dealing with the
frogs and salamanders in the United States began to appear. These may well have
stimulated the interests of budding herpetologists, and the field expanded. A list
of herpetologists, most of whom were still active when it was published in 1974,
indicated about 800 in the United States, 36 in Canadá, but only 1 in México
(where there were at least 3). Not all of these were devoting their efforts to research,
but a fair percentage had published at least one report.

Until 1936 only one joumal published in the United States provided an outlet
for scientific contributions from herpetologists, and this Journal was shared with
ichthyologists. For the last 25 years, however, three journals have been available
in the United States and a few in other countries. There are, of course, joumals
of animal behavior, ecology, and other disciplines that also publish the results of
investigatíons dealing with amphibians. Hundreds of such reports appear annually,
in addition to books restricted to specialized investigatíons such as the results of a
1976 symposium that dealt only with the reproductive biology of amphibians.

We need only tum back to an earlier summary to discover how much more we
know about amphibians today than half a century ago. G. Kingsley Noble in his
authoritative Biology of the Amphibia (1931) suggested that the frogs, toads, and
salamanders now living included only some 1900 species. The caecilians were so
poorly known that the only figure Noble mentioned represents about a third of
the species now recognized. Noble's estímate, therefore, would have approximated
fewer than 2000 species. When William E. Duellman and Linda Trueb completed
their survey of the literature summarized in the present book, their estímate of the
total was nearly double that of Noble. In other words, systematísts studying the
amphibians have been adding ñames to the roster of valid species at an average
rate of 37 species per year.
Not all of the species added have necessarily been discovered or even recognized
for the first time. A large percentage of them have nevertheless been diagnosed,
described, and validly named since 1931. A good many others, however, had
been erroneously assigned to subspecific status or even synonymized by students
who had underevaluated the extent of the differentiation. In some instances, spe-
cies represented by populations incapable of interbreeding had been viewed as
belonging to one species. For example, tree frogs occupying similar habitats on
opposite sides of the southwestern deserts in the United States and superficially
similar morphologically were regarded as being conspecific for over half a century.
Not until portable tape recorders became available in the 1950s had anyone at-
tempted to subject the tree frogs' matíng calis to scientific analysis using audio-
spectrograms. These spectrograms revealed such profound differences that no one
has since doubted that two distantly related species are represented. Inevitably
field studies disclosed significant differences in the species' modes of reproduction.

Satisfactory solutions to innumerable taxonomic problems awaited the introduc-

tion of new ideas, new concepts, new methods, and new or better equipment.
Intensive field investigations revealed differentiation in behavioral traits as well as
adaptive specializations that discouraged or prevented interbreeding between am-
phibians that earlier workers had regarded as being morphologically indistinct.
Truly satisfactory solutíons to some problems of relationships awaited the use of
electrophoresis or detailed knowledge of mechanisms of inheritance. Geneticists,
partícularly Theodosius Dobzhansky and his students, tumed their attention to
xii
 Foreword
species problems, and devised experimente that paved the way to significant im-
provements in the systematists' concept of the species, Taking their cues from
Dobzhansky, systematists were soon discussing "closed systems" and carrying out
field investigations to ascertain which "isolation mechanisms" discouraged or pre-
vented interbreeding when related species were sympatric.

The more enlightened systematists realized that their predecessors had depended
far too heavily on the examinatíon of preserved specimens. Even though taxon-
omists had refined their techniques of measuring, recording, and evaluating
morphological characters, the better systematists realized that such information
could be interpreted far more effectively if correlated with the resulte of ecological
and ethological investigations in the field. Ways were devised to supplement field
studies with breeding experimente carried out under controlled laboratory condi-
tions, perhaps more easily with some frogs than with highly specialized amphibians.
Anatomical studies remained important, of course, and systematists continued to
rely heavily on the maintenance of extensive collections of well-documented spec-
imens. These are required not only to deal with the problems of variations but to
document distributions. Only the most conservatíve taxonomists regarded collec-
tions with the philosophy of the stamp collector, who acquired only one of each
kind. The acquisition of extensive broadly representative collections by large mu-
seums became the sine qua non of "the new systematics." It became important
to students of evolution to find out whether populatíons of closely related animáis
lived side by side or occupied sepárate ranges or habítate. Ernst Mayr undoubtedly
clarified the thinking of systematists and other students of evolution when he coined
the terms allopatric and sympatric.

Merely poinüng out that the class Amphibia proves to be represented by at least
twice the number of species that an authority recognized in 1931 may seem off-
hand to be of limited significance. Even if systematists continued to recognize
additional species of caecilians, frogs, and salamanders at current rates, which is
most improbable, they would require anothej- century to double the representation
of amphibians. The new systematics, however, is not restricted to morphological
descriptions. Students of evolution, perhaps more than other specialists, have con-
tributed to the synthesis of the many fields now recognized. We have witnessed
the interdigitatíon of anatomy, physiology, ecology, ethology, endocrinology, and
paleontology, to mention only a few disciplines. There is, therefore, a sound basis
for the assumption that advances in our knowledge of the biology of the amphib-
ians in its widest sense closely parallel those that have broadened our understand-
ing of the composition of the class Amphibia.

Paradoxically, the proliferation of humans that led to the exploitatíon of rain-

foreste may already be contributing to the decline of the amphibians. We are
informed that the rainforeste of the world are being destroyed at rates averaging
approximately 30 acres for every minute of every day. Once comprising 2.4 billion
acres of prime amphibian habitat, the rainforeste are being converted irretrievably
into useless wasteland. The frogs, salamanders, and caecilians finely adjusted to
this environment are being destroyed, and species may be extínguished.

Herpetologists must struggle with the abundance of information, oíd and new.
Some find time to examine the more impressive "classics"—multivolumed, some-
times lavishly illustrated accounts that began to appear even before Linnaeus's
day—but usually can only sample. Herpetologists feel inundated by the flood of
information rolling off the presses. As early as 1950 no one could even pretend
to read everything published that pertained to amphibians and reptiles, even if all
such publications were accessible. At least the oíd card Índex to the literature that
passed through the herpetologist's hands—a laborious system with title cards typed
by the secretary and organized according to subject—can be superseded by mod-
ern retrieval systems.
Xlll
Foreword
Regardless of how capable, well informed, or experienced, a herpetologist is
unlikely to assume the responsibility of preparing a Biology ofAmphibians without
the support and encouragement of a sympathetic institution. Fortunately William
E. Duellman and Linda Trueb are among the very few, either here or abroad,
who have the requisite qualifications, including the ambitíon and efficiency, to
summarize virtually all learned thus far about the caecilians, salamanders, and
frogs. At least, nearly everything confidently regarded as pertínent has been in-
cluded. This account is not a compendium or an encyclopedia. Nearly every chap-
ter could be expanded to fill an entire volume. What students as well as practicing
herpetologists, biology professors, and even enlightened laypersons are likely to
prefer is a reasonably complete but concise account of a fairly large, widely dis-
tributed group of animáis. This is what Linda Trueb and William Duellman, after
years of work in the field, in the library, and in the laboratory and classroom, have
managed to produce.

The University of Kansas, which has long and faithfully supported herpetological
research, along with study collections, also deserves credit. Duellman and Trueb,
whether working independently or as a team, in recent decades have been among
the most efficient and productive herpetologists in the United States. Anyone who
makes full use of this book is unlikely to question this appraisal.
CHARLES M. BOGERT
Santa Fe, New México
March 1985

XIV
Nearly a decade has passed since the publication of Bio/ogp ofAmphibians by the
McGraw-Hill Book Company. The decisión by that publisher not to reprint the book
left the biological community in a dilemma, because Bio/ogy of Amphibians had
become the standard reference in the field and has also been used as a text in courses
at many universities. The copyright was transferred to us by McGraw-Hill, who also
provided the original production films of the text. Shortly thereafter, we arranged
with the Johns Hopkins University Press to reprint Bio/ogy of Amphibians in this
soft-cover edition; with the exception of the cover, this preface, and Figure 13-16,
which is reproduced correctly herein, this book is identical to the original edition.

We are sympathetic with the reader who had hoped for a revisión of the original
text. Indeed, an update and revisión would be a timely and significant contribution,
but we cannot undertake such an onerous task at this time. Moreover, had the origi-
nal films not been used to produce this volume, the price of the book would have
increased tremendously. In what we hope will be an acceptable compromise, we
provide herein references to major works that substantially supplement or modify
information presented in the original edition of Bio/ogy ofAmphibians. The follow-
ing comments are organized sequentially according to the chapters in the book.

The historical resume (Chapter 1) is not particularly outdated. However, readers

who wish more information about amphibian biologists who are now deceased
should consult the detailed, illustrated biographies of 152 herpetologists by K. Ad-
ler, 1989, "Herpetologists of the past," in K. Adler (ed.), Contributions to the His-
tory o/Herpeío/ogy, Contributions to Herpetology, No. 5, Oxford, Ohio: Society
for the Study of Amphibians and Reptiles.

xv
Preface
During the past decade much has been written about reproductive strategies in
amphibians (Chapter 2). One of the most important papers is that of R. A.
Nussbaum, (1985, The evolution of parental care in salamanders, Mise. Publ. Mus.
Zoo/. Univ. Michigan, 169:1-50). Nussbaum argued that the sex that chooses the
oviposition site will be the care-giving sex, and that the sequestering of sper-
matophores from courtship sites by females of some species determines that the
females of these species will be the care-giving sex.

We originally devoted 21 pages to the subject of vocalization (Chapter 4). This

material has been expended greatly with respect to the structure, function, and evo-
lution of the auditory system by 28 authors in a book of 705 pages: B. Fritzsch, M. J.
Ryan, W. Wilczynski, T. E. Hetherington, and W. Walkowiak (eds.), 1988, The Evo-
lution of the Amphibian Auditory System, New York: John Wiley and Sons.

The biology of larval amphibians (Chapter 6) continúes to be an exciting field.

By defining a dichotomy between the sources of energy used during larval
development—endotrophy and exotrophy—R. Altig and G. Johnson (1988, Guilds
of anuran larvae: relationships among developmental modes, morphologies, and
habits, Herpetol. Monogr., 3:81-109) contributed significantly to our understand-
ing of the biology of larval anurans. Based on their comprehensive survey of anuran
larvae, these authors offered speculative scenarios and hypotheses concerning the
functional adaptations of different larval morphologies and the relationships of
trophic structures to the ecology of the tadpoles.

Chapter 7 provides fíindamental information on the complex mechanisms gov-

erning metamorphosis in amphibians. The ecological and evolutionary implica-
tions of amphibian metamorphosis, along with processes of its control, are bur-
geoning fields of contemporary research that, as yet, have not been reviewed
synthetically. However, the evolution of metamorphosis in amphibians with respect
to the brain stem, inner ear, and lateral-line system, was reviewed in the context of
adaptive changes by B.Fritzsch (1990, The evolution of metamorphosis in amphib-
ians, J. Neurobio/., 21:1011-1021). Fritzsch argued persuasively that changes trans-
forming tadpoles into froglets evolved within amphibians and, contrary to popular
wisdom, that the process of metamorphosis in amphibians does not reflect the
water-to-land transition of ancient amniotes.

The material on relations with the environment (Chapter 8) should be augmented

by the excellent reviews of ecological and developmental physiology included in
M. E. Feder and W. W. Burggren (eds.), 1992, Environmental Physiology of the
Amphibians, Chicago: University of Chicago Press. Much new material is presented
in the section on energetics and locomotion, and the section on development and
reproduction is also pertinent to Chapter 2 (reproductive strategies) and Chapter 5
(eggs and development).

The major new information that bears on population biology (Chapter 11) is the
observation by biologists that populationsof many species of amphibians through-
out the world have declined since the mid-1980s. Much of this decline can be attrib-
uted to destruction or modification of habitats, but the decline of populations in
pristine áreas suggests that more subtle (and as yet, unidentified) causes are respon-
sible. Declining populations are not evident in all taxa in all locations, ñor is there
evidence of a single global causal factor. The issue was addressed at a workshop
sponsored by the National Research Council, USA, in February 1990. A summary
was published as "Declining amphibian populations—a global phenomenon?
Findings and recommendations," Alytes, 9:33-42. Subsequently, the Species Sur-
vival Commission of the International Union for the Conservation of Nature estab-
lished the Declining Amphibian Populations Task Forcé, which is coordinating re-
search on monitoring amphibian populations.

xvi
 Preface
Several ¡mportant publications that deal with community ecology and species
diversity (Chapter 12) have appeared recently. Foremost with respect to herpeto-
faunal communities in neotropical rain foreste are five chapters dealing with four
long-term study áreas and a comparative summary in A. H. Gentry (ed.), 1990,
Four Neotropical Rainforests, New Haven: Yale University Press. Species diversity
of neotropical frogs was summarized by W. E. Duellman, 1988, Patterns of species
diversity in anuran amphibians in the American tropics, Ann. Missouri Bot. Gard.,
75:79-104. Diversity of anurans in África and South America was analyzed by
W. E. Duellman, 1993, "Amphibians in África and South America: evolutionary
history and ecological comparisons" in P. Goldblatt (ed.), BiologicalRelationships
Between África and South America, New Haven: Yale University Press. The latter
reference also is pertinent to biogeography (Chapter 18). On a smaller, but far more
in-depth, scale is the thorough work by N. G. Hairston, 1987, Community Ecology
and Salamander Guilds, Cambridge: Cambridge University Press, in which the au-
thor emphasizes different dynamics among communities of pond-breeding, stream-
side, and terrestrial salamanders.

Readers interested in the morphology of amphibians (Chapters 13 and 14) are

directed to The Skull (J. Hanken and B. Hall [eds.], 1993, Chicago: The University
of Chicago Press); the three volumes that comprise the series (Vb/ume 1: Develop-
ment; Volunte 2: Patterns ofStructural and Systematic Diversity; Vb/ume 3: Func-
tional and Evolutionary Mechanisms) represent a synthesis of the comparative mor-
phology, development, evolution and functional biology of the vertébrate skull. A
great deal of valuable information on fossil and recent amphibians is integrated into
many of the chapters.

There are several useful supplements and updates to the discussion of primitive
tetrapods and their relationships (Chapter 15). J. A. Gauthier, A. G. Kluge, and
T. Rowe (1988, "The early evolution of the Amniota" in M. J. Benton [ed.], Am-
phibians, Reptiles, Birds, The Phyhgeny and Classification of Tetrapods, Vol. 1.
Oxford: Clarendon Press.) examined which taxa among extinct tetrapods are re-
lated most closely to the Amniota. In another chapter of the same work, A. Mllner
("The relationships and origin of living amphibians") reviewed the status of each of
the orders of living amphibians. The most recent treatment of the relationships of
primitive tetrapods is Section I of a book edited by H. P. Schultze and L. Trueb
(1991, Origins of the Higher Groups of Tetrapods: Controversy and Consensus,
Ithaca, New York: Cornell University Press.); seven authors contributed five chap-
ters dealing with the origin of tetrapods. The systematic status and relationships of
living amphibians are extensively dealt with by three authors in two chapters in the
same volume (op. cit.). John R. Bolt reinvestigated the positions of the dissorophids
and the microsaurHapsidopareion with respect to the Lissamphibia, and, in a major
phylogenetic study based on osteological features and soft-anatomical characters,
L. Trueb and R. Cloutier attempted to document the monophyly of the Lissam-
phibia and hypothesized relationships between this group and primitive tetrapods.

Persons interested in cytogenetic, molecular, and genomic evolution (Chapter

16) should consult the volume, Amphibian Cytogenetics and Evolution, edited by
D. M. Green and S. K. Sessions (1991, New York: Academic Press, Inc.). This book,
which consiste of 17 chapters contributed by 24 authors, is a vital source that largely
supersedes our treatment of the subjects. Also, the material on chromosome com-
plemente has been expanded by M. Kuramoto, 1990, A list of chromosome num-
bers of anuran amphibians, Bu//. Fufcuoka Univ. Education, 39:83-127.

Significan! advances have been made in our understanding of the phylogenetic

relationships of some groups of amphibians (Chapter 17). Use of molecular data has
resulted in the formulation of altérnate hypotheses of the relationships of the fam-
ilies of salamanders (A. Larson, 1991, A molecular perspectiva on the evolutionary

xvii
Preface

relationships of the salamander families, Evol Biol., 23:211-277); both molecular

and morphological data support the recognition of the Rhyacotritonidae (D. A.
Good and D. B. Wake, 1992, "Geographic variation and speciation in the torrent
salamanders of the genus Rhyacotriton [Caudata: Rhyacotritonidae]," Univ. Cal-
ifornia Publ Zoo/., 126:1-91). Caecilians have been subjected to a thorough phy-
logenetic analysis by R. A. Nussbaum and M. Wilkinson, 1989, On the classification
and phylogeny of caecilians (Amphibia, Gymnophiona), a critical review, Herpetol.
Monogr., 3:1-42. Although the phylogenetic relationships among most of the fam-
ilies of neobatrachians remain unresolved, progress continúes in the resolution of
relationships among the archaeobatrachians; see D. C. Cannatella and L. Trueb,
1989, Evolution of pipoid frogs: morphology and phylogenetic relationships of
Pseudhymenochirus, J. Herpetol., 22:439-456, and papers cited therein.

The classification of amphibians (Chapter 19) has changed greatly during the past
few years as the result of the discovery of new species and genera, reallocation of
taxa to different higher categories, and even the recognition of more families. The
taxonomy has been updated through 1992 by W. E. Duellman, 1993, Amphibian
species of the world: additions and corrections, SpecialPubl. Mus. Nat. Hist. Univ.
Kansas, 21:1-372. Thus, while living amphibians formerly were classified in 36
families, 397 genera, and 3925 species, now 41 families, 428 genera, and 4522
species are recognized. Some of these taxonomic changes and associated phy-
logenetic analyses have an impact on the biogeographic scenarios (Chapter 18).

We hope that the foregoing brief synopsis of recent pertinent literature will pro-
vide an entrée into the specialized literature on particular topics. Furthermore, this
material clearly demónstrales that the interrelated disciplines involving the biology
of amphibians continué to be a dynamic and exciting field of endeavor.
WILLIAM E. DUELLMAN AND LINDA TRUEB
Lawrcnce, Kansas
May 1993
 Preface to First Edition

More than half a century has passed since the publication of G. K. Noble's Biology
of the Amphibia, in 1931. Noble's book has been the primary source for infor-
mation on amphibians; understandably, it is out of date now. For many years we
have taught a course on the biology of amphibians and have become increasingly
frustrated by the lack of an adequate text. Furthermore, we have been exasperated
by the number of hours spent tracking down some trivial facts, as well as syn-
thesizing major blocks of information for use in lecture or publication.

With the urging and blessings of many of our colleagues we began early in 1980
to prepare the manuscript for this book. We have endeavored to produce a book
that will serve not only as a text in a course designed for advanced undergraduate
and gradúate students but as a reference for amateur and professional biologists
interested in diverse aspects of amphibian biology—from paleontology to physi-
ology, from genetics to community ecology, with the coverage worldwide. We
hope that we have succeeded.

In the organizatíon, there are two lengthy chapters (2 and 3) on structure. Chap-
ters 2 through 5 deaí with diverse aspects of reproduction, and Chapters 6 and 7
are concerned with larvae and metamorphosis. Chapters 8 through 12 are con-
cerned with the relationships of amphibians with their environment—biotic and
abiotic. Chapters 13 and 14 examine the morphology of amphibians. The evo-
lutionary history of amphibians is treated in Chapters 15 and 16, whereas Chapters
17 and 18 are concerned with the phylogeny and biogeography of the modern
groups of amphibians. Chapter 19 contains a definitíon of each of the families,
summary of the fossil history, generalized treatment of the life history, statement

xix
Preface to First Edition
of geographic distributíon, and a list of all recognized generic ñames, together with
generic synonyms, numbers of recognized species, and distributíon.

Some readers may be concemed that there are no chapters devoted to behavior
or to locomotion. These subjects are covered in appropriate places. For example,
behavior is discussed in relation to reproduction, courtship, vocalizatíon, larvae,
physiological ecology, feeding, and enemies. Likewise, not all aspects of structure
are covered in Chapters 13 and 14; for example, the structure of the sound-
producing mechanism of anurans is discussed in the chapter on vocalizatíon, and
the structure of the feeding mechanisms is treated in the chapter on feeding. Any
of these subjects can be located through the use of the índex.

Throughout the book we nave stressed function and evolutíon. Thus, in the
chapters dealing with morphology, we have tried to discuss structure with respect
to functional systems. We have emphasized the evolutionary significance of aspects
of reproduction, development, physiology, and ecology. Most chapters (or appro-
priate sections therein) begin with a discussion of the conceptual framework in
which the material is presented, and most chapters termínate in a discussion re-
lating the material to broader aspects of amphibian biology.

We have endeavored to choose appropriate examples worldwide to ¡Ilústrate

our points. Thus, a person knowledgeable about the amphibian fauna of Australia,
Brazil, Europe, or West África will find as many familiar examples as will the person
in North America. Of course, there are limitations. For example, most of literature
concerned with endocrinology, development, or physiology deals with a relatíve
few North American or European species.

Although we have depended heavily on our own personal knowledge of am-

phibians that has accumulated during a combined 60 years of experience, much
of the information presented in this book has been taken from the vast and ex-
panding literature. For those disciplines with which we were not particularly familiar
we have relied on syntheses and summary papers (when available). Moreover, we
have tried to include the latest information on all subjects. Thus, of the more than
2500 references (in 12 languages) cited, about one-third have appeared since we
began working on the manuscript less than 5 years ago.

References are cited in the text by author and date; in cases of publications
having two authors, both ñames are given. If there are more than two authors,
only the first author is given followed by et al. Instances of different authors with
the same súmame are distinguished by first (and sometimes second) initials. All
authors Usted by ñame in the text are referenced in the Índex.

We have endeavored to update the taxonomy throughout the text. Current

seientific ñames are used; these are not necessarily the ñames that were used in
publications that are cited. All generic and specific ñames used in the text, tables,
and illustrations are included in the índex.

We owe a great debt of gratitude to many persons throughout the world for
aiding us in innumerable ways. First and foremost we are indebted to our daughter,
Dana Trueb Duellman, who while developing from an adolescent girl to a midteen
tolerated our countless hours of labor and helped to manage our household.

We have shamelessly called upon many colleagues for information and refer-
ences. Many persons have provided us with photographs and tape recordings;
each is acknowledged in appropriate legends. Innumerable investigators have pro-
vided us with manuscripts (some unsolicited) in an effort to keep us up to date.

xx
 Preface to First Edition
We are especially grateful for critical reviews of the chapters (noted in parenthe-
ses) by Kraig Adler (1), Stevan J. Arnold (3), Thomas J. Berger (6, 11, 12), James
P. Bogart (16), Charles M. Bogert (1), Ronald A. Brandon (6, 7), Bayard H.
Brattstrom (8), Edmund D. Brodie, Jr. (10), Daniel R. Brooks (10), David C.
Cannatella (13, 15, 17, 19), Martha L. Crump (2, 12), Richard Estes (15, 17, 19),
Linda S. Ford (8, 13), Darrel Frost (1, 17, 18, 19), John S. Frost (16), Sally K.
Frost (2, 5, 7, 14), Cari Gans (4, 9), David M. Hillis (16), Robert Holt (12), Robert
G. Jaeger (9, 11), Harvey Lillywhite (8), Murray Littlejohn (4), John D. Lynch
(13, 17, 19), Linda R. Maxson (16, 18), Roy W. McDiarmid (3), Charles W. Myers
(10), Ronald A. Nussbaum (17, 19), Rebecca A. Pyles (9, 13), Rodolfo Ruibal (8,
14), Stanley N. Salthe (5), Jay M. Savage (17, 18, 19), Hans-Peter Schultze (15,
18), Norman J. Scott, Jr. (12), Catherine A. Toft (9), Frederick B. Turner (11),
David B. Wake (9, 13, 17, 18, 19), Marvalee H. Wake (9, 13, 14, 17, 18, 19),
Richard J. Wassersug (6, 7), Kentwood D. Wells (2, 3, 4), Ernest E. Williams (15),
and Richard G. Zweifel (5). In additíon, Robert C. Drewes and Michael J. Tyler
reviewed material on Australian and African anurans, respectively. Their efforts
have greatly increased the accuracy and presentation of the material. However,
any errors of omission, commission, and interpretation are our solé responsibility.

Our colleagues at the University of Kansas have suffered during the past 5 years.
We are especially grateful to Sally K. Frost and Hans-Peter Schultze for the use
of their personal librarles. We thank the personnel in the Science Library for aid
in tracking down elusive references and in obtaining others on interlibrary loan.
Production of the manuscript was made less painful by the typing skills of Rose
Etta Hermann, Jennifer Volpe, and Bernard Willard. We are especially grateful to
Rebecca A. Pyles for managing the computer files; the entire manuscript was
processed on remote termináis to the Academic Computing Center. Nearly all of
the photographs were processed by John E. Simmons, whose efforts and skills in
the darkroom are greatly appreciated. Lastly, we are grateful to Patricia A. Bur-
rowes for her assistance in compiling the índex.

We would be remiss if we did not acknowledge our past and present gradúate
students who have contributed so much, both directly and indirectly, to the real-
ization of this project. Basically they have provided the stimulus for our undertaking
the work. They have been a continuing source of encouragement on one hand,
and our most severe and exacting critícs on the other. We hope that the final
product meets their expectations, and we dedícate this book to them with our
profound gratitude.
Sybil P. Parker, Joe Faulk, and Edward J. Fox of the Professional and Reference
División of the McGraw-Hill Book Company are professionals in the truest sense
of the word. We express our appreciation to them for their continued support and
expertise in bringing our efforts to fruition.

Finally, each of us owes a debí of gratitude to the persons who introduced us

to the fascinating world of amphibians. For one of us (Duellman), the late Charles
F. Walker of the University of Michigan provided continuous challenges and en-
couragement to investígate the biology of amphibians, a group of organisms that
were very special for him. Perhaps it is a break in traditíon to acknowledge an
undergraduate zoology course, but were it not for a stimulating and comprehensive
introduction to the world of vertébrate natural history at the University of California
at Berkeley, the second author (Trueb) doubtless never would have pursued grad-
úate studies in herpetology. She extends her thanks to Robert C. Stebbins who
introduced the new horizon and to Daniel C. Wilhoft who, through his enthusiasm
and interest, encouraged her to investígate it.
WILLIAM E. DUELLMAN AND LINDA TRUEB
Lawrence, Kansas
October 1984
XXI
 Biology of
Amphibians
 CHAPTER 1
These foul and loathsome animáis are
abhorrent because of their cold body, palé
color, cartilagíneas skeleton, fllthy skin,
fierce aspect, calculating eye, offensive
smell, harsh voice, squalid habitation, and
terrible venom; and so their Creator has
not ejcerted his powers to make many of
them.
Caro/us Linnaeus (1758)

s "ince Linnaeus's early misconceptions about am-

phibians, biologists have discovered that these animáis
are among the most fascinating and numerous of terres-
and pituitary hormones has come from endocrinological
studies on amphibians. Likewise, the ease of breeding
amphibians in the laboratory and their relatively simple
trial vertebrales. From the time of their remarkable feat chromosome complements have provided bases for im-
of colonizing the land in the Mid-Devonian, nearly 350 portant advances in studies of hybridizatíon and specia-
million years ago, amphibians have evolved a wide range tion. The vocalizations of frogs have provided a means
of morphological and ecological types. Of these, the three for studying acoustic communication and, together with
living groups—frogs, salamanders, and caecilians— con- other aspects of courtship and mating, have presented
tain more than 3900 living species, and new species (and the evolutionary biologists with a wealth of material for
even new genera) are being discovered each year. studies on sexual selection. These are but a few selected
examples of the exciting ways in which studies of am-
phibians are contributing to knowledge of biology and
THE WORLD OF AMPHIBIANS our understanding of biological phenomena.
Amphibians are intermedíate in some ways between the The term amphibian can be interpreted in two ways—
fully aquatic fishes and the terrestrial amniotes. However, either as an animal spending part of its life in water and
they are not simply transitíonal in their morphology, life then changing to an aquatic adult, or as an animal that
history, ecology, and behavior. In the successful attain- alternates life in and out of water, such as so-called pond
ment of independence from water and colonizaüon of frogs. Actually both interpretations are valid in part but
land, amphibians have undergone a remarkable adaptive neither applies to all amphibians, some of which are aquatic
radiation, and the living groups exhibit a greater diversity throughout their Uves, but others of which neither enter
of modes of life history than any other group of verte- water ñor have aquatic stages in their life histories. So,
brales. Their shell-less eggs have been studied exten- what sort of animal qualifies as an amphibian?
sively by developmental biologists, and much of the basic Essentially, amphibians can be defined as quadrupedal
knowledge of vertébrate embryology is based on am- vertebrales having two occipital condyles on the skull and
phibians. The metamorphosis from aquatic larvae to ter- no more than one sacral vertebra. The skin is glandular
restrial adults has been the subject of intensive studies, and lacks the epidermal structures (scales, feathers, hair)
and much of what is known about the actions of thyroid characteristíc of other groups of tetrapods. Although some
Introduction to the Amphibia
Paleozoic amphibians were large, plated quadrupeds, most used in their narrow sense; in referring to all frogs and
living amphibians are small. The largest salamander at- toads, the ordinal derivativo anuran is used.
tains a total length of about 1500 mm, whereas the larg-
est frog is about 300 mm. Caecilians reach a length of
about 1500 mm. Caecilians and some salamanders lack HISTORICAL RESUME
limbs and girdles, and in some other salamanders these In order to place present knowledge of amphibian biol-
structures are reduced. In frogs the postsacral vertebrae ogy in perspective, we provide a brief history of the field
are fused into a single rodlike element, the coccyx, the of herpetology with emphasis on those workers who are
tail is absent, and the hindlimbs are elongated and mod- major contributors to knowledge of amphibian biology.
ified for jumping. Although epidermal scales are absent This review is biased in favor of those workers who are
in amphibians, dermal scales are present in the skin of herpetologists and therefore neglects many of the inves-
most caecilians. The skin is highly glandular and contains tigators who as physiologists, embryologists, or bio-
both mucous and granular (poison) glands. Truc claws chemists also have made important contributions.
are absent, but horny tips are present on the toes of some As biology emerged as a science in the late 1600s and
frogs and salamanders. early 1700s, amphibians played an important role in re-
Internally, the strucrure of living amphibians is inter- search. For example, the first descriptíon of cleavage in
medíate between that of fishes and amniotes. The heart a zygote was of a frog egg by Jan Swammerdam (1738).
has two atria, a single ventílele (which may be partíally It is noteworthy that in the same year that Linnaeus's
divided), and a distínct conus arteriosus with several valves. (1758) tenth edition of the Systema Naturae, which rep-
The aortic arches are symmetrical. Typically, amphibians resents the foundation for subsequent zoological nomen-
have two lungs, but the lungs are reduced in some sal- clature, was published, Rósel von Rosenhoft (1753-58)
amanders and absent in one entíre family (Plethodonti- published a superbly illustrated folio on the life history of
dae). The left lung is greatly reduced in most of the elon- European frogs with special emphasis on Rana escu/enta
gate caecilians (as it is in snakes). Living amphibians also and thereby provided the first detailed documentation of
have some unique characters. They all have pedicellate the amphibian egg, aquatic larva, and morphological
teeth and specialized papillae in the inner ear, and sala- transformation into the terrestrial adult.
manders and anurans have green rods in the retina of During the latter part of the 18th century and through-
the eye. out most of the 19th century, the principal occupation of
The life histories of amphibians are highly diversified. biologists was collecting and classifying organisms. In the
Most species of frogs have externa! fertilization, whereas late l700s, París became the center for herpetological
internal fertilization occurs in the majority of salamanders research. Frangois Daudin (1802) published the first
and presumably in all caecilians. The classic amphibian comprehensive account of frogs; as part of the ency-
life history of aquatic eggs and larvae, although typical clopedic "Suites de Buffon," Daudin (1803) summarized
of many frogs and some salamanders, is only one of the existíng knowledge on amphibians in volume 8 of
many modes of reproduction, which include direct de- Histoire Naturelle, Genérale et Particuliére des Reptiles.
velopment of terrestrial eggs (no aquatic larval stage), The encyclopedic coverage of amphibians was expanded
ovoviviparity, and even viviparity. All amphibian eggs considerably in a later edition of the "Suites de Buffon";
must develop in moist situations, for although they have Andre M. Constant Duméril, Gabriel Bibron, and Au-
numerous protecüve mucoid capsules, these capsules are guste H. A. Duméril (1841, 1854) covered amphibians
highly permeable. The eggs lack a shell and the embry- in two volumes of the Erpétologie Genérale ou Histoire
onic membranes (amnion, allantois, and chorion) of higher Naturelle Complete des Reptiles. Meanwhile in Switzer-
vertebrales. In those amphibians that have aquatic lar- land, Johann J. von Tschudi (1838) attempted a classi-
vae, the larvae undergo metamorphosis into the adult fication of living and fossil amphibians, and in Vienna,
form; this is an especially drámatic change in frogs. Leopold Fitzinger (1843) proposed a classification of am-
The terms Urodela and Apoda are sometimes used phibians and reptiles; many currently used generic ñames
instead of Caudata and Gymnophiona for salamanders were proposed by these workers. Toward the middle of
and caecilians, respectively, whereas in some literature the 19th century, the center of herpetology shifted to
Salientia is used interchangeably with Anura for frogs. London, where Albert C. L. G. Günther at the Britísh
Even common English ñames become confusing. It is not Museum (Natural History) published an important sys-
uncommon in the literature to find "salamanders and tematic treatise and catalogue of amphibians in that mu-
newts" or "frogs and toads." Newts are aquatic members seum in 1859. Large quantiües of natural history material
of the family Salamandridae, and are salamanders. Like- were added to the collections of the Britísh Museum
wise, at least in the narrow sense, toads are members of through the energetíc efforts of Britísh explorers and col-
the family Bufonidae, and are frogs in the broad sense. lectors during Britain's great period of colonizatíon. These
Thus, all newts are salamanders, but not all salamanders formed the bases for many publicatíons by Günther's
are newts, and all toads are frogs, but not all frogs are successor, George A. Boulenger (Fig. 1-1), whose major
toads. To avold confusión, the terms newt and toad are contributions include the catalogues of the anurans (1882a)
 Introduction to the Amphibia

Figure 1-1. Major workers and pioneers in

various disciplines of amphibian biology: upper
left, George Albert Boulenger (courtesy of the
British Museum [Natural History]); upper right,
Edward Drinker Cope (courtesy of the Academy
of Natural Sciences of Philadelphia); lower left,
Ernst Gaupp (from Anatomische Anzeiger, vol.
49, 1917); lower right, Gladwyn K. Noble
(courtesy of American Museum of Natural
History).

and of the salamanders and caecilians (1882b) and the these are especially evident in his works on frog classifi-
detailed studies on the European anurans (1897-98). cation (1865) and on the amphibians of North America
Other important contributions were made in the field (1889).
of amphibian taxonomy in the latter part of the 19th Although Cope pioneered in the use of internal mor-
century by Frangois Mocquard and Paul Brocchi in France, phology in the classification of amphibians, it was the
Wilhelm Peters and Osear Boettger in Germany, and J. von Germán anatomists of the 19th century who provided
Bedriaga in Russia. However, the preeminent student of excellent descriptive anatomy accompanied by superb
amphibians of the time was Edward D. Cope (Fig. 1-1), illustrations. Johannes Müller (1835) discovered that cae-
who was associated with the Academy of Natural Sci- cilians had gilí slits and were in fact amphibians, not snakes.
ences in Philadelphia. Cope's prodigious writings encom- Robert Wiedersheim (1879) published on the anatomy
passed the fields of vertébrate paleontology and anat- of caecilians; this was followed by the detailed work on
omy, ichthyology, and herpetology. In addition to his the development and morphology of ¡chthyophis gluti-
multitudinous papers describing new taxa, Cope's major nosas by Paul and Fritz Sarasin (1887-90). Probably the
contributions were in the utílization of internal morpho- most detailed and copiously illustrated works on am-
logical characters, partícularly the skeleton, in determin- phibian anatomy are those by C. K. Hoffmann (1873-78)
ing the relationships of and in classifying amphibians; that dealt with all groups of amphibians, and those of
Introduction to the Amphibia
Ernst Gaupp (Fig. 1-1) on the development and anatomy phibian life histories, his Amphibians of Western China
oí anurans, culminating in his Anatomie des Frosches (1950), and his work in collaboration with Shu-quing Hu,
(1896). Also at this time in England, William K. Parker Tailless Amphibians of China, published in 1961. Studies
completed several major works on amphibian osteology. on amphibians in China are continuing, especially by
By the early years of the 20th century, several centers Shu-quing Hu and Ermi Zhao and their associates at the
of herpetology were established in various parts of the Chengdu Institute of Biology. A modern account of the
world, and in many of these emphasis was on amphibi- amphibians of Taiwan was prepared by G.-Y. Lúe and
ans. Despite two world wars, amphibian research contín- S.-H. Chen (1982). In the Philippines, Ángel C. Alcalá
ued to flourish in Europe. At the British Museum (Natural at Silliman University has provided thorough studies of
History) in London, Hampton W. Parker conünued Cope's the life history and development of Philippine anurans.
tradition of careful morphological studies concerned with Indian herpetologists have concentrated on morphol-
amphibian classification, an approach subsequently ogy and development. Especially noteworthy are the
maintained by Alice G. C. Grandison. At the Museum studies on caecilians by L. S. Ramaswami and on anu-
National d'Histoire Naturelle in Paris, various herpetol- rans by Beni C. Mahendra. The only comprehensive sur-
ogists under the influence of Fernand Ángel and Jean vey of the amphibians of Sri Lanka was written by
Guibé pursued investigations on the amphibians of West P. Kirtisinghe (1957).
África and Madagascar, and Alain Dubois is now working Although most of the early work on Australian am-
on Himalayan anurans, Jean Lescure on South American phibians was done by British herpetologists, in the 1880s
anurans, and Jean-Paul Risch on Asian amphibians. In the Australians developed a center of study at The Aus-
Italy, Giuseppe Cei (Fig. 1-2) initíated importan! studies tralian Museum in Sydney, with J. J. Retcher being the
on reproductive cycles; these were followed by similar foremost Australian worker on amphibians. By the 1950s,
investigations on salamanders by V. Vilter and his asso- A. R. Main and his students were actively studying the
ciates in France and were extended to viviparous frogs systematics, ecology, and life histories of frogs in Western
by Máxime Lamotte and his associates. In Denmark, Arne Australia. One of Main's students, Murray J. Littlejohn,
Schi0tz (1967, 1975) has made importan! contributions established another center at the University of Mel-
to the knowledge of anurans in tropical África; these have bourne, and with his collaborators, including Angus A.
been augmented by many importan! works on the am- Martin and Graeme F. Watson, has been innovative in
phibians of West África by Jean-Luc Perret in Switzerland the use of bioacoustics and hybridization in the study of
and Jean-Luc Amiet in Cameroon. The Belgians estab- speciation of anurans. Michael J. Tyler's tireless efforts at
lished an intensive program on the biota of the Congo seeking out previously unknown frogs has resulted in the
at the Musée Royal du Congo Belge in Tervuren; Ray- discovery of many new species in Australia and New
mond F. Laurent made many important contributions on Guinea; now at the University of Adelaide, he is collab-
the amphibians. In the Netherlands, research emphasized orating with Margaret Davies on systematic revisions of
the amphibian faunas of the Dutch East Indies (Indonesia), the Australo-Papuan anurans.
especially by P. N. van Kampen (1923), and currently In South America, studies on amphibians lagged behind
on Surinam by Marinus S. Hoogmoed and on Mada- other parts of the world. Prior to World War II, two Bra-
gascar by Rose M. A. Blommers-Schlósser. zilians made important contributions. Alipio de Miranda-
The study of amphibians, especially anurans, has flour- Ribeiro of Sao Paulo published a beautifully illustrated
ished in South África in the 20th century. At Stellenbosch book on Brazilian frogs in 1926. Although a physician by
University, C. G. S. de Villiers and C. A. du Toit and trade and a parasitologist by profession, Adolpho Lutz
their students carried out detailed morphological studies. contributed many works on the taxonomy of Brazilian
Investigations on the systematics, distribution, and life frogs; his investigations were conünued by his daughter,
histories of anurans have culminated in several impor- Bertha Lutz, whose efforts culminated in her 1973 work
tant works by Walter Rose (1962), J. C. Poynton on the Brazilian tree frogs of the genus Hy/a. At the Mu-
(1964), V. A. Wager (1965), and N. I. Passmore and seu Nacional in Rio de Janeiro, Antenor Leitao de Car-
V. C. Carruthers (1979). valho made important contributions to knowledge of
The Japanese have had a long history of study of am- Brazilian amphibians, especially microhylid frogs. Knowl-
phibians. Yaichiro Okada's (1931) beautifully illustrated edge of the diversity of Brazilian frogs has been increased
work on the anurans of the Japanese Empire and Ikio greatly by the systematic investigations of Werner C. A.
Sato's (1943) work on the salamanders of Japan pro- Bokermann in Sao Paulo and Eugenio Izecksohn in Rio
vided an Ímpetus for investigations by many successors. de Janeiro. The fascinating frog fauna of températe South
Work on amphibian genetics and development is accom- America has been studied by José M. Gallardo and Av-
plished at the Laboratory for Amphibian Biology estab- elino Barrio in Buenos Aires; the latter made especially
lished at Hiroshima University in 1967 by Toshijiro Ka- important contributions to studies of anuran speciation
wamura (Fig. 1-2). Other important works by biologists through bioacoustic and karyological investigations. After
in eastern Asia include Rene Bourret's (1942) Les Batra- World War II, Giuseppe Cei moved from Italy to Argen-
ciens de l'Indochine, Ch'eng-chao Liu's work on am- tina and as José Cei established an important center at
 Introduction to the Amphibia

Figure 1-2. Recent workers in the field of

amphibian biology: upper left, John A. Moore
(courtesy of J. A. Moore); upper right, José M.
Cei (photo by W. E. Duellman); lower left,
Toshijiro Kawamura (courtesy of T. Kawamura);
lower right, W. Frank Blair (courtesy of
University of Texas).

Mendoza, where he continued work on reproductive knowledge of the systematics of Venezuelan (1961) and
cycles, initiated studies on immunological relationships, Puerto Rican (1978) frogs.
and completed major works on the amphibians of Chile By the early part of the 20th century, several important
(1962) and Argentina (1980). Likewise, Raymond F. centers of herpetology had been established in the United
Laurent immigrated to Argentina and at the Fundación States. First, programs were developed at the Museum
Miguel Lillo in Tucumán has continued to make impor- of Comparatíve Zoology at Harvard University and the
tant contributions to the systematics of frogs. National Museum of Natural History in Washington. At
By comparison with Brazil and Argentina, the number the National Museum, Leonhard Stejneger was respon-
of herpetologists in other South American countries has sible for a growing collectíon of international importance.
been relatively few. Jehan Vellard, working at the Museo He was followed by Doris M. Cochran, who devoted her
Javier Prado in Lima, completed several major works on life to the study of frogs from the American tropics and
the frogs of Andean Perú. Alberto Veloso M. and Ramón published major works on Hispaniola (1941), southeast-
Formas in Chile have been productive in studies of the ern Brazil (1955), and (with Coleman J. Goin) on Col-
taxonomy, karyology, and life histories of Chilean frogs. ombia (1970). Currently, aspects of the systematics and
Pedro M. Ruíz-C. and his associates in Bogotá have in- behavioral ecology of neotropical anurans are being in-
itiated promising studies on the anurans of Colombia. vestigated at the National Museum by W. Ronald Heyer
Juan A. Rivero has made significan! contributions to and Roy W. McDiarmid; George R. Zug is contributing
Introducüon to the Amphibia
studies on anuran locomotion. Biogeographic and sys- At Comell University, Albert H. Wright initiated a tra-
tematic studies of amphibians flourished at Harvard un- dition of research on the natural history of anurans; many
der the magnanimous influence of Thomas Barbour. One of the students at Comell (e.g., Sherman C. Bishop, James
of his students, Emmet R. Dunn, provided significant in- Kezer, Karl P. Schmidt) became well-known investigators
sights into amphibian relatíonships; Dunn is best known in various disciplines of amphibian biology. An active
for his classic work on the plethodontid salamanders program in physiological ecology, neurobiology, and be-
(1926b). Arthur Loveridge of Harvard wrote extensively havior continúes with research by Kraig Adler, Robert R.
on the amphibians of East África. Currently at the Museum Capranica, and F. Harvey Pough.
of Comparative Zoology, Pere Alberch has an active pro- Somewhat later three other herpetological centers were
gram on the evolutionary morphology of amphibians. founded. The Field Museum of Natural History in Chi-
Also, early in this century three other centers were cago has had an active role in amphibian systematics and
developed. The establishment of the Museum of Zoology biogeography initiated by Karl P. Schmidt and continued
at the University of Michigan by Alexander G. Ruthven by Robert F. Inger, who has made many significant con-
initiated one of the most active centers of gradúate train- tributions to knowledge of the anurans of southeastern
ing in herpetology and included such important person- Asia and adjacent archipelagos. At the University of Kan-
ages as Frank N. Blanchard, Helen T. Gaige, Norman E. sas, Edward H. Taylor made prodigious contributions to
Hartweg, Grace L. Orton, Laurence C. Stuart, Frederick the field of herpetology, including comprehensive works
H. Test, and Charles F. Walker. Present workers at the on amphibians of the Philippines (1920), Costa Rica
University of Michigan include Cari Gans in the field of (1952), Thailand (1962), and (with Hobart M. Smith)
functional morphology, Arnold G. Kluge and Ronald A. México (1948); Taylor also produced the only mono-
Nussbaum working on systematics and evolutionary graph of the caecilians (1968). Present research at Kansas
ecology, and George W. Nace, who established a labo- emphasizes anurans, with William E. Duellman working
ratory for maintaining genetic stocks of amphibians. on the systematics of neotropical frogs, especially hylids
The American Museum of Natural History in New York (1970), and anuran communities (1978), Linda Trueb
has maintained an active program of studies on amphib- working on evolutionary morphology (1973) and sys-
ians since the early work by Mary C. Dickerson (1906) tematics of anurans (1970a), and Sally K. Frost studying
on the frogs of North America. She was followed by amphibian pigmentation. Studies on amphibians at the
Gladwyn K. Noble and Clifford H. Pope, who worked University of California at Berkeley have emphasized sal-
on Chínese anurans and North American salamanders. amanders, especially in the investigations of Robert C.
Later Charles M. Bogert was one of the pioneers in the Stebbins and David B. Wake and their students; these
investigation of anuran vocalizatíons (1960) and an im- studies have included diverse aspects of life history,
portant contributor to knowledge of the systematics of ecology, speciation, and evolutionary morphology.
the amphibians of México. Presently at the American Mu- The latter field is emphasized in caecilians by
seum, Richard G. Zweifel is a leader in the field of de- Marvalee H. Wake.
velopmental ecology of amphibians and a specialist on These long-established centers of research on amphib-
Australo-Papuan frogs; Charles W. Myers (with his co- ian biology continué to be important; gradúate training
worker John Daly) has been innovative in the use of programs have continued to be active at these univer-
biochemical propertíes of skin toxins combined with more sities. Research at other institutions has flourished and
traditional taxonomic characters in the study of dendro- waned or has begun more recently, depending on the
baüd frogs. investigators associated with them. Sherman C. Bishop
Gladwyn K. Noble (Fig. 1-1) received training in her- at the University of Rochester was the foremost student
petology, taxonomy, and biogeography under the tute- of eastern North American salamanders; his major works
lage of Thomas Barbour at Harvard University and later (1941, 1943) influenced a generation of students. George
obtained his doctor's degree at Columbia University un- S. Myers had an active gradúate and research program
der the guidance of William K. Gregory. Fortunately for on systematics of amphibians and reptiles at Stanford
the institution and his chosen field, Noble became curator University in the 1940s and 1950s; with Myers's retire-
of the Department of Amphibians and Reptiles at the ment, the program terminated and the important collec-
American Museum of Natural History. Noble was far ahead tions were added to those at the California Academy of
of his time in the application of experimental methods to Sciences, where Robert C. Drewes maintains an active
problems of life history and behavior, and he founded research program on the systematics and physiological
the Department of Experimental Biology (later known as ecology of African anurans. While at Columbia University
the Department of Animal Behavior) at the museum. in the 1940s and 1950s, John A. Moore (Fig. 1-2) carried
During his relatively short career, he integrated aspects out important studies on the development and physiol-
of life history into the study of phylogeny and introduced ogy of amphibians, and published a pioneer treatise on
experimental methods into studies of amphibian ecology the anurans of Australia (1961). At the University of Texas,
and reproduction. His Biology of the Amphibia (1931b) W. Frank Blair (Fig. 1-2) pioneered studies of speciation
has been the standard reference on amphibian biology of anurans using nonmorphological data, especially vo-
for more than half a century. calization and hybridization; this work by Blair and his
 Introduction to the Amphibia
students culminated in a book on evoluüon in the genus Presently, research on amphibian biology is under way
Bu/o (1972). Jay M. Savage, formerly at the University by hundreds of investigators at institutions throughout the
of Southern California and now at the University of Miami, world. Many of these researchers are highly specialized,
has maintained an active program in the study of system- and their research varíes from alpha taxonomy and de-
atícs and biogeography of amphibians for a quarter of a scriptive morphology to feeding ecology and the bio-
century. At the University of Florida, Coleman J. Goin chemistry of egg capsules; in many instances the research
and his students made major contributions to the knowl- involves only a single species. However esoteric some of
edge of systematics and life histories of amphibians of this research may seem, it all contributes to an accu-
the southeastern United States and the Caribbean región; mulation of knowledge that eventually can be interrelated
now Martha L. Crump of the same institution is active in and synthesized to present a more accurate, comprehen-
the field of evolutionary ecology of anurans. The mor- sive understanding of biológica! phenomena and princi-
phology, physiology, and behavior of tadpoles has been pies, with particular reference to amphibians. In recent
studied by Richard J. Wassersug and his students for- years, the major attempts at syntheses have been the
merly at the University of Chicago and now at Dalhousie results of symposia, such as those on the evolutionary
University in Halifax, Canadá. biology of anurans (Vial, 1973) and on the reproductive
Although fossil anurans and salamanders received some biology of amphibians (D. Taylor and Guttman, 1977);
attenüon in the last century, the major research on fossils or of compilations of works by many specialists, such as
has occurred since the mid-1950s by numerous workers, those on amphibian physiology edited by Moore (1964)
particularly Walter Auffenberg, Richard Estes, Coleman and Lofts (1974, 1976), on the amphibian visual system
J. Goin, Max K. Hecht, J. Alan Holman, Charles Mesz- edited by Fite (1976), on the neurobiology of frogs edited
oely, Bruce Naylor, and Joseph A. Tihen in North Amer- by Llinás and Precht (1976), and on metamorphosis ed-
ica; Francisco de Borja Sanchíz, Oskar Kuhn, Jean-Paul ited by Gilbert and Frieden (1981). The only modern
Rage, Zbynek Rocek, and Zdenek Spinar in Europe; Ana comprehensive checklist of amphibians was the result of
María Báez and Osvaldo A. Reig in South America; and efforts by amphibian biologists worldwide (D. Frost, 1985).
Eviatar Nevo in Israel. Landmark publications on fossils
include the work on Tertiary frogs of Europe by Spinar
(1972) and the handbook of fossil salamanders and cae- PROSPECTS FOR THE FUTURE
cilians by Estes (1981). Studies of amphibian biology promise to be exciting for
Early in the 1900s, Hans Spemann and his associates many decades in the future, provided that political, en-
in Germany determined the role of the dorsal lip of the vironmental, and regulatory activities do not hinder
blastopore of frog embryos as an organizer, and in France, investigations.
Jean Joly and his associates experimented with early de-
velopment of salamanders. At about the same time in Research
the United States, W. H. Lewis's work on the induction Many challenges confront biologists studying amphibi-
of the lens of the eye in Rana and T. H. Morgan's ex- ans. Although descriptive morphology reached its heights
periments on limb regeneration in salamanders were classic in the last century, much important work still needs to be
contributions to the understanding of tissue interactions done. The basic morphology of only a handful of am-
during development. Tissue culturing was developed at phibian species is known. Comparative morphological
Yale University by Ross G. Harrison using Ambystoma studies combined with analyses of functions will provide
maculatum, the species for which he prepared a detailed the data necessary for understanding the evolutionary
staging table. One of his students, Víctor C. Twitty (1966), significance of morphological features. Likewise, knowl-
integrated experimental biology with studies of speciation edge of the developmental programs of morphological
and behavior of newts (Taricha) in California. W. Gardner units is necessary for a meaningful interpretation of the
Lynn (1942) made important contributions through his evolutionary sequences with respect to heterochrony.
studies on direct development in amphibians. Summaries The limited information available on water balance,
of the use of amphibians in embryological studies were temperature tolerances, and ion balance in amphibians
provided by one of the foremost investigators in the field, indicates that these animáis are far more complex phys-
Roberts Rugh (1951, 1962). Beginning with J. F. Gun- iologically than is generally believed. Many more studies
dernatsche's (1912) discovery of the effect of thyroxin integrating physiological tolerances, metabolic rates, and
on metamorphosis of Rana, amphibians have played an behavior are necessary before generalities can be made
important role in research on experimental endocrinol- about metabolic levéis and foraging activities or escape
ogy; this work has been summarized by Lawrence I. Gil- behavior. Most of these kinds of studies necessitate the
bert and Earl Frieden (1981). The colony of axolotls maintenance of animáis in captivity; in recent years suit-
(Ambystoma mexicanum) established at the University able techniques have been devised for maintaining and
of Rochester (now maintained at Indiana University) by breeding amphibians in captivity (Schulte, 1980; J. Frost,
Rufus R. Humphrey has provided a reliable source of 1982; Mattison, 1982).
material for investigations in embryology, endocrinology, Since the mid-1970s, discoveries of previously unsus-
and genetics. pected reproductive behavior suggest that many fasci-
Introduction to the Amphibia
8 nating aspects of reproductive biology remain to be dis- that the greatest diversity of anurans occurs. Second are
covered. However, the most rewarding prospects will be hydrologic controls that affect wetlands, habitáis used for
the integration of diverse reproductive behavior, me- breeding by many amphibians. Innumerable populations
tabolism, and environmental factors. of amphibians in Europe and the Middle East have been
Genetic studies of amphibians are still in their infancy. decimated by the elimination of breeding sites (Honeg-
New techniques of protein synthesis and DNA hybridi- ger, 1981), and populations of amphibians have been
zation, as well as many approaches now in use, should threatened seriously in such extensive wetland áreas as
continué to provide new kinds of data on the transmis- the Everglades in southern Ronda (L. Wilson and Porras,
sion of traits and on the relationships of living popula- 1983).
tions. Population genetics combined with demographic The second major threat to amphibians is pollutíon,
data are desirable to provide an understanding of how principally the accumulation of biocides in the environ-
populations exist in nature and what factors affect their ment. Extensive use of insecticides and herbicides with
stability. These kinds of data, together with information residues that contamínate the soil and water are highly
about reproductive biology, will establish a basis for detrimental to amphibians. Aquatic eggs and larvae are
meaningful ecological studies. Amphibian biologists need particularly susceptible to these toxic substances, as well
to shake off the dogma of community studies done on as acid rain, which may not occur in concentratíons suf-
birds and approach amphibian communities with an open ficient to kill adults or even embryos; nevertheless, sev-
mind. eral toxic substances do affect the development of em-
At one and the same time, systematic biology is con- bryos and larvae to the point of causing a high percentage
sidered to be the basis and the ultímate synthesis of biol- of abnormalities or a decrease in the rate of development
ogy; yet nowhere is the fragmentary nature of knowledge resultíng in prolonged larval periods or dwarfed young
of amphibians more apparent than in the classificatíon of (Judd, 1977; Mohanty-Hejmadi and Dutta, 1981; Dun-
amphibians that attempts to represen! the phylogeny of son and Connell, 1982). The great increase in the use
the living groups. In part, this is because of the very of fertilizers and biocides in developing countries, espe-
incomplete fossil record, which continúes to improve cially in the tropics, has potentially disastrous effects on
slowly. Nearly one-third of the known species of am- amphibian populations. Amphibian eggs and larvae are
phibians have been named only since the mid-1960s. especially sensitive to heavy metáis; drainage from mines
Probably the numbers of recognized species will continué can have calamitous effects on some populations of am-
to increase dramatically as collectors forage in previously phibians (Porter and Hankason, 1976).
unknown áreas of the world and as more refined tech- The introductíon of exotic species of amphibians has
niques are used to define species. been minimal in comparison with introductions of other
As the research on amphibians increases, so does the groups of vertebrates. Too little is known about the ef-
literature, which has amounted to more than 1000 titles fects of introductions, but to date no native species of
per year listed in the Zoohgical Record since 1970. It is amphibian is known to have become extinct because of
not feasible to keep up to date on more than a small the introduction of an exotic species. Even the introduc-
fraction of the literature. Therefore, most biologists will tion of the African clawed frogXenopus laevis into south-
have to rely on papers summarizing and synthesizing re- ern California seems to have had no deleterious effect
cent developments in the field. Furthermore, computer- on the native biota (McCoid and Fritts, 1980). Also, there
ized data banks are a necessity for storage and retrieval is no evidence that the introduction of Bufo marinus in
of information. southern Florida has been detrimental to the native toads
(L. Wilson and Porras, 1983). However, these auíhors
Conservaron and Regulation suggested that the introduced tree frog Osteopilus sep-
Throughout the history of civilization, human activities tentrionalis, which eats other frogs, may be affecting pop-
have been detrimental to the natural biota. As human ulations of two species of native tree frogs, Hyla cinérea
populations have increased dramatically, especially in the and H. squirella. On the other hand, the introduction of
last half century, more and more environmental destruc- exotic fishes can be highly detrimental to native amphib-
tíon has eliminated natural habitat and modified the en- ians. Tyler (1976) considered the introduction of Gam-
vironment on such a large scale that many species are in busia and Tilapia to be a major threat to the eggs and
danger of extinction. Although amphibians seldom are tadpoles of Australian anurans.
the subject of direct eradication, they are affected indi- Ordinarily amphibians are collected for: (1) commer-
rectly and often disastrously. cial purposes to be used as food, as aquarium animáis,
The first major threat to populations of amphibians is in teaching, or in zoo exhibits, and (2) scientific investi-
habitat destruction. This is particularly evident in two ways. gation purposes. Compared with other groups of verte-
First is the clearing of forests, especially those in the hu- brates, relatively few amphibians are collected for com-
mid tropics. At the present rate of clearing, most of the mercial purposes. However, commercial collecting of some
humid tropical forests of the world will have been de- species of frogs, especially Rana escalenta and R. ñdi-
stroyed by the end of this century. It is in these forests bunda in Europe, must put heavy pressures on some
 Introduction to the Amphibia
populations. For example, Honegger (1981) provided tries (or even states) additional species are considered to 9
statistics to show that more than 2,000,000 of these frogs be rare or endangered, and collectíng is restricted or for-
were exported as a luxury food item from Greece in bidden. For example, under the Endangered Species Act
1975. Likewise, imports of frogs for food into Switzerland of the United States, as of 1983, eight species of anurans
ranged from 995,000 to 1,800,000 individuáis per year and five of salamanders are listed as endangered and
between 1976 and 1980. Numerous exotic species of one species of anuran and two of salamanders are listed
amphibians are collected for the pet trade; commercial as threatened. The regulations in many countries and
dealers of amphibians are principally in western Europe, states or provinces within countries have little, if any,
where terrarists are especially plentiful. sound biological basis, and in many instances, ill-consid-
Scientific collectíng of amphibians results in far fewer ered laws have created serious impediments to funda-
individuáis being taken than are gathered by commercial mental research.
collectors. Most scientists are fully aware of the potential There is little chance that human pressures on natural
threats of overcollecting and take only the number of populations of plants and animáis will diminish in the
individuáis necessary for their scientific work. Since the foreseeable future. Governments throughout the world
early 1970s, agencies in governments throughout the have the resources for the establishment and mainte-
world, as well as international organizations, have at- nance of limited numbers of natural preserves. These
tempted to define some of the problems regarding nat- preserves should incorpórate natural áreas of high en-
ural populations of animáis and have passed legislation demicity and should be of sufficient size to preserve nat-
regulating the perturbation of these populations. Com- ural populations of the entíre biota (Lovejoy, 1982). Fur-
pared to well-known and popular big game animáis and thermore, reserves should be designed not only for the
many kinds of birds and reptiles, amphibians have been protection of the habitat and the communities residing
nearly ignored in efforts to protect individual species. As therein but also for scientific investigation. If such pre-
of 1983, only 5 species of salamanders and 12 species cautions are taken, the next generation of amphibian
of anurans are controlled by the Conventíon on Inter- biologists will still be able to study frogs, salamanders,
national Trade in Endangered Species of Wild Fauna and and caecilians in nature and not have to rely solely on
Flora (CITES). However, levéis of protection of various preserved specimens and the writings of earlier generations.
species differ from country to country, and within coun-
 PART

LIFE HISTORV
 CHAPTER
The variation [in reproductiva behavior] ís
a mirror ofthe environmental difficulties
that have been overeóme, and
demónstrales a wíde variety ofsuccess
storíes.
Michael J. Tyler (1976)

A Ln essential attribute of any surviving species or

populaüon is the ability to produce a succeeding genera-
2. Fecundity, including number and size of eggs,
frequency of oviposition, and proportion of
tion. Classically, ideas concerning reproduction in am- females breeding.
phibians have centered on North Températe species of 3. Duration of development, including proportion
salamanders, such as Ambystoma and Triturus, and anu- of time spent as feeding larvae.
rans, such as Bu/o and Rana, most of which undergo 4. Age at first reproduction and reproductive life
brief, annual periods of mating and leave unattended span.
eggs to develop into aquatic larvae. This pattern of re- 5. Reproductive effort, including parental care.
production is unknown in caecilians and is common to 6. Quantitative and environmental constraints.
probably no more than a quarter of the living species of
salamanders. Although this generalized pattern occurs in Studies on amphibians reveal considerable disparity
a wide variety of anurans, a great diversity of reproduc- between theory and empirical evidence. Most data are
tive patterns exists among the frogs and toads. Indeed, qualitative or are limited to few parameters. Very little is
no general statement can be made about reproductivo known about caecilians (M. Wake, 1977a). As a group,
patterns in amphibians. the salamanders are better known than the anurans, prin-
A reproductivo strategy may be viewed as the com- cipally because most of the species of anurans that have
bination of physiological, morphological, and behavioral diverse reproductive modes live in the tropics, where few
attributes that act in concert to produce the optimal num- detailed studies have been accomplished. The most com-
ber of offspring under certain environmental conditions. prehensive review of reproduction in amphibians is by
Reproductive strategies are as significant to the survival Salthe and Mecham (1974). M. Wake (1982) reviewed
of the species as are physiological and morphological the diversity of reproductive modes within morphological
adaptations to the environment. Patterns of reproduction and physiological constraints.
are modified by natural selection so as to produce strat-
egies with high fitness, and they reflect a compromise
among many selective pressures. Some components of REPRODUCTIVE CYCLES
reproductive strategies are: Reproductive cycles in amphibians are subject to hor-
monal controls, which within genetic limitations respond
1. Endogenous and extrinsic controls of game- to environmental variables and produce certain patterns;
togenetic cycles. further constraints are imposed by the organism's micro-
13
LIFE HISTORY
habitat, size, reproducüve mode, and parental care prac- gonocytes and give rise mitotically to successive genera-
tices. General patterns are evident: (1) Caecilians repro- üons of oocytes. Primary oocytes undergo meiotic divi-
duce biennially. (2) Salamanders reproduce annually or sión to yield secondary oocytes and the first polar bodies.
biennially. (3) Anurans in the wet tropics have continuous A subsequent reduction división of the secondary oocyte
reproduction and may deposit several clutches of eggs results in an ovum and a secondary polar body. The ova
per year; in seasonally dry or cold regions, their cycles are surrounded by a discrete cell membrane, a narrow
are interrupted and the number of clutches may be as zona pellucida, and a single layer of follicle cells. Previ-
few as one per year or one every other year. (4) Deflnite tellogenic oocytes increase in size nearly tenfold; nutri-
relattonships exist between body size and clutch size within ents for this growth are provided by the ovary vía plas-
reproductive modes. (5) Annual fecundity varíes from ma membranes forming the follicular stalk (Wallace
one or two to potentially more than 80,000 offspring. et al., 1970).
The process of vitellogenesis is the accumulation in the
Gametogenesis cytoplasm of the oocyte of a supply of nutrients for em-
The development and maturation of the sex cells in am- bryonic development (Follett and Redshaw, 1974). These
phibians are well known and adequately discussed and nutrients, collectively referred to as yolk, consist of about
illustrated in most texts on embryology. A thorough, well- 45% phosphoproteins, 25% lipids, and 8% glycogen (Barth
documented review of gametogenesis in salamanders and and Barth, 1954). In Rana temporaria the oocyte grows
anurans (Lofts, 1974) was supplemented by M. Wake's during a period of three years; most of the 27,000-fold
(1968, 1977a) work on caecilians. increase in size in these comparatively telolecithal eggs
The spermatogenetíc cycle is completed in the testes. occurs in the six months prior to ovulation (P. Grant,
The testes are simple, ovoidal structures in anurans and 1953). The proporüonal increase in the macrolecithal eggs
most salamanders, but they are composed of lobes in of amphibians having direct development would be much
some salamanders (desmognathines and Neotropical greater. In amphibians having definitive reproductive
plethodontids) and all caecilians. In salamanders the cycles, four distínct stages of oocytes and ova may be
number of lobes may increase with age; in caecilians the distinguished at the beginning of the breeding season
number remains unchanged after sexual maturity is at- (Lofts, 1974): (1) numerous cell nests that will provide
tained. During spermatogenesis each lobe is character- the generation of follicles for the subsequent spawning;
ized by the presence of a number of dilated lobules. In (2) previtellogenic follicles from which succeeding gen-
caecilians each lobule contains sperm cells in different erations of eggs will be recruited; (3) rapidly growing
stages of maturation. Within a single lobule, clusters of vitellogenic follicles that are rapidly adding nutrients; and
cells may range from primary spermatogonia to maturing (4) fully grown postvitellogenic ova.
spermatids (M. Wake, 1968). In salamanders each of the Among most amphibians, oocytes normally have only
individual locules contains sperm cells in the same stage one nucleus. However, there are some exceptions among
of maturation, but along the length of the tesüs there is anurans. Oogénesis in Ascaphus truel regularly involves
a developmental gradient representing successive zones oocytes with eight nuclei; all but one disappear before
of spermatogonia, spermatocytes, spermatids, and ma- the final stages of oogénesis (Macgregor and Kezer, 1970).
ture spermatozoa; the anterior lobes are least advanced Multinucleate oocytes occur in 11 of 33 species of egg-
sexually. In multilobed testes the developmental spec- brooding hylids examined by del Pino and A. Humphries
trum occurs within each testicular lobe (Lofts, 1974). (1978); all are species that produce few eggs (all macro-
The structurally simple testes of anurans increase in lecithal). In one of these, F/ectonotus pygmaeus, small
size and weight during spermatogenesis. In températe oocytes contain 1,000-3,000 nuclei; the number de-
anurans the sperm cells mature uniformly throughout the creases gradually in larger oocytes until only one nemains
testis (Lofts, 1974), but in tropical species that breed in the mature ovum. The other egg-brooding hylids have
throughout the year, the testes contain sperm cells in far fewer nuclei in their early oocytes. The multínucleate
various stages of maturation. For example, in Rana condiüon seems to develop through the disappearance
erythraea in Borneo, each locule contained sperm cells of cell membranes between adjacent cells within a cyst.
in only one stage of maturation, but the locules in one Nuclei in the outer shell of oocytes are larger than those
tesüs often contained cells in all stages of spermato- in the inner part, and the larger ones contain more ri-
genesis (Inger and Greenberg, 1963). The termination of bosomal DNA. Macgregor and del Pino (1982) suggested
the period of spermatogenesis is characterized by various that the nucleus with the highest ribosomal DNA content
changes in the testes, including increase in interstítial tis- may be the one to survive in the germinal vesicle.
sue, disintegration of lobule stromata, degeneration of
intralobular ducts, and presence of only a few sperma- Endogenous Factors
tocytes peripherally in the lobules. The seasonal development and activity of the male and
Oogénesis is basically the same in all three groups of female gonads are under the direct control of the ade-
amphibians. The developing ova lie in follicles associated nohypophysis (pars distalis of the pituitary), which in turn
with the ovary. Oogenia are derived from primordial is regulated by the central nervous system mediated via
 Reproductive Strategies
hypothalamic neurosecreüons transported to the pituitary Some valuable information has been accumulated (but 15
gland in the portal vessels (Jorgensen, 1974). The ex- not necessarily published) about reproduction of certain
tensive literatura on experimental endocrinology and am- species in the laboratory. Ambystoma mexicanum will
phibian productivo cycles was reviewed by C. L. Smith mate with no exogenous stimulation from November
(1955), van Oordt (1960), and Lote (1974). through early April in the Northern Hemisphere; during
There is a positive correlation between the secretion a given season females are capable of producing several
of pituitary gonadotropin and seasonal changes in the clutches of eggs, and males produce large numbers of
germinal epithelium and secondary sexual characteristics spermatophores. Pleurodeles walti reproduces every 4 to
in male anurans and male salamanders. Ablation of the 8 weeks in the laboratory. In the spring and fall, breeding
entire pituitary or only the pars distalis results in atrophy in Rana pipiens can be induced by pituitary extraéis, but
of the reproductive organs; hypophysectomy results in only if the extract is from R. pipiens or another member
atrophy of the ovaries and secondary sexual character- of that species complex. Unsuspecting researchers that
istics in females. Androgenic hormone production by the are supplied í?. berlandieri in place of R. pipiens often
interstitial tissue in the testes diminishes during the re- are frustrated in their attempts to induce ovulation;
productive season. Limited experimental data suggest that R. berlandieri will breed only in the summer. Bombina
a gonadal feedback regulating gonadotropic production orientalis can breed year-round when stimulated with
by the pars distalis exists in both sexes (van Oordt, 1961; anuran pituitary extracts or human chorionic gonadotro-
Rastogi and Chieffi, 1970; Vijayakumar et al., 1971). pin; Xenopus laevis responds every 2 or 3 months to the
Three types of pituitary cells may provide hormonal same hormome. Injections of the synthetic hormone
control of reproductive activity: B2 basophilic cells with (D-Ala6, des-GlylO)—LHRH ethylamide (Helix Bio-Tec
luteinizing effects, B3 basophilic cells with follicle-sSmu- Ltd.) provides a stimulus to the pituitary causing it to
lating activity, and Aj acidophilic cells with luteotrophic reléase hormones inducing ovulation and spermatoge-
effects. In the températe toad Bufo bufo, the proportions nesis; múltiple breeding has been so induced in anurans
of these three kinds of pituitary cells change during the as diverse as Ceratophrys omata, Bufo marinus, and Li-
reproductive season (Obert, 1977). The Aj cells decrease toria caemlea (E. Wagner, pers. comm.).
slightly in number; the number of B2 cells is greatly re- Experimental laboratory studies have provided sub-
duced, and the B3 cells become much more numerous. stantial evidence for the hormonal control of reproductive
Androgenic hormone production by the interstitial tissue cycles, and numerous studies have shown the correlation
in the testes diminishes during the reproductive season. of environmental factors with breeding activity in am-
Limited experimental data suggest that a gonadal feed- phibians. However, knowledge of how extrinsic factors
back regulating gonadotropic production by the pars dis- influence endogenous controlling mechanisms remains
talis exists in both sexes (van Oordt, 1961; Rastorgi and limited.
Chieffi, 1970; Vijayakumar et al., 1971).
In oviparous amphibians, postovulatory follicles are Extrinsic Factors
transient and apparently have no hormonal function In general, hormonal activity, such as secretion by the
(Redshaw, 1972); the presence of corpora lútea in ovo- adenohypophysis, is correlated with environmental
viviparous salamanders and frogs and in viviparous cae- changes. These changes act as primary stimuli to nerve
cilians (M. Wake, 1977a), the salamander Salamander receptors and are integrated by the central nervous sys-
otra (V. Vilter and A. Vilter, 1964), and the toad Nec- tem, which relays appropriate impulses to the hypotha-
tophrynoides ocrídentalis (Lamotte et al., 1964) is as- lamic neurosecretory nuclei. Spermatogenetic cycles are
sociated with hormonal secretions differing from those in essentially continuous in tropical and subtropical am-
other amphibians. Extensive studies on the viviparous phibians and in some cave-dwelling species in températe
N. occidentalis reveal that the corpora lútea produce pro- regions. The cycle is interrupted or impaired during the
gesterone, which acts with estrogen during the follicular autumn and winter in most températe species and during
phase of oogénesis, but acts alone in the luteal phase; the drier or colder seasons in some high montane species
furthermore, progesterone inhibits embryonic develop- in the tropics. This discontinuity is correlated directly with
ment during maternal aestivation (Lamotte and Rey, 1954; the negative effect of lower temperatures on the secretion
Xavier, 1970, 1973, 1977; Xavier et al., 1970). There is of gonadotropin by the pituitary and the sensitivity of
evidence of ovarían control of incubation and pouch vas- germinal epithelium to gonadotropic hormones. Sper-
cularization in the marsupial frog, Gastrotheca riobam- matogenetic and ovarían cycles are not necessarily syn-
bae, in which postovulatory follicles may correspond chronous and, therefore, may be influenced by different
functionally to corpora lútea in maintaining early incu- internal or externa! factors.
bation (del Pino and Sánchez, 1977). In this species, Temperature apparently is the major factor controlling
pouch formation can be induced in juvenile females by gametogenesis in many salamanders. Temperatures of
administration of estrogen (R. E. Jones et al., 1973). more than 20° are necessary to initiate spermatogenesis
Many kinds of amphibians are commonly used for de- in Plethodon rínereus (Werner, 1969) or ovulation in
velopmental and endocrinological studies in laboratorios. Cynops pyrrhogaster (Tsutsui, 1931). Temperatures of
LIFE HISTORY
more than 12° can cause degeneration of spermatocytes growth in Xenopus laevis (Holland and Dumont, 1975).
and spermatids (Ifft, 1942). The correlation of seasonal Evidence also exists for innate sexual rhythms that are
temperature variaüon and spermatogenesis was dem- genetically controlled and not under direct environmen-
onstrated experimentally in Plethodon cinéreas (Wemer, tal-hormonal influence. In ffana temporaria, the germinal
1969) and Paramesotriton hongkongensis (Lofts, 1974). epithelium enters into a quiescent period that begins in
Rainfall seems to be the primary factor initíating breed- late summer when temperatures are high and lasts through
ing activity in amphibians. Series of observations and the winter (Witschi, 1924). The germinal epithelium re-
experiments on anurans in the Chacoan región of north- mains relatively insensitive to high temperatures and high
ern Argentina, which is characterized by a distínct rainy levéis of gonadotropin induced experimentally during the
season, revealed differential responses to temperature (see early part of the period (van Oordt, 1956). Similar in-
Cei, 1980, for review). Conünuous spermatogenesis and sensitivity of the germinal epithelium to increased tem-
mature oocytes were observed in 13 species, but lower peratures during the early part of the quiescent period
winter temperatures inhibited gonadotropic effects on the was noted in Plethodon cinerus (Werner, 1969). Also,
germinal epithelium. Spermatogenesis is impaired nota- autonomous spermatogenetic cycles occur in Rana ar-
bly during the winter in three other species; in one, the valis and R. dalmatina (Cei, 1944). Spermatogenesis is
ovarles become atresic, but in the other two, mature oo- continuous in some lowland populations of Salamandra
cytes are present throughout the year (Cei, 1949b). Sim- salamandra, but spermatozoa are present in the Wolffian
ilarly, spermatogenesis is retarded in Phyllomedusa sau- ducts only during 3 months in the summer (Joly, 1960b).
vagei in the winter, when it aesüvates (Caruso, 1949). In the salamandrid Pleurodeles walti, maintained under
The differences in the sexual cycles exhibited by two constant laboratory conditions, females are capable of
sympatric species of Leptodactylus are especially signifi- breeding throughout the year, but males will mate only
can!; L. ocellatus shows no seasonal variation in game- during September through May (Pastisson, 1963). In the
togenetíc activity, whereas in L. chaquensis both sper- Upemba área of tropical West África, maturation of the
matogenetic and oogenetic cycles are inhibited by low ova in Bu/o funéreas and B. regulañs is correlated with
temperatures (Cei, 1948, 1950). Moreover, conünued the rainy season, but the nuptial excrescences in males
exposure to high temperatures results in a cessation of of B. regulañs develop immediately before the beginning
spermatogenesis in L. chaquensis (Rengel, 1950). Some of the rainy season and regress before the end of the
high montane frogs that are subjected to year-round cold rainy season (Inger and Greenberg, 1956). Thus the cyclic
temperatures maintain conünuous spermatogenesis; this development of nuptial excrescences presumably is con-
has been documented in the Andean Hyla pulchella (Ca- trolled genetically.
ruso, 1949) and in the aquatic Andean Telmatobius hau- Seasonal changes in secondary sexual characters are
thali, which is active at temperatures of 6-8°. notable in many amphibians, but these seem to be under
It is unlikely that photoperiod is very important in the hormonal control. For example, Noble (1931a) reported
regulation of sexual cycles in amphibians that are noc- on male hormonal control of the development of caudal
turnal or trióse that remain underground when inactive. glands in Desmognoíhus fuscus. Nuptial excrescences and
However, spermatogenesis was advanced experimentally male throat coloration were developed experimentally by
in Plethodon cinéreas during the latter part of the quies- hormonal injections in juveniles and female Bu/o wood-
cent period and during early spermatogenesis by increas- housii fowleri (P. Blair, 1946). Testosterone control of
ing the daily duration of light (Werner, 1969). The lunar the development of mental glands and cirri in Eurycea
cycle has been implicated in the rhythm of ovulation in quadridigitata was shown experimentally by Sever (1976).
Bu/o me/anostíctus in Java, where the species breeds The cyclic nature of most, if not all, secondary sexual
throughout the year; at times of a full moon, more ovu- characteristics probably is influenced by the pituitary-
lating females are found than in darker phases of the gonadal axis. Secondary sexual characters are discussed
moon (Church, 1960a). In nature, Pachymedusa dac- more fully in Chapter 3.
nicolor breeds only in the summer, and adults maintained
in a greenhouse in Tucson, Arizona, deposited múltiple Annual Patterns
clutches over a period of 3 months (July—September). If The innate gametogenetic cycles, acting within con-
day length and temperature are manipulated so as to straints of the local environment, produce annual pat-
decrease and then to increase, simulating summer con- terns of reproductive cycles. Additional constraints are
ditions, the frogs breed spontaneously again in December imposed on some species by specialized modes of repro-
through early February (S. Frost, pers. comm.). duction and investment in parental care (see following
The nutritional status of females may affect the num- sections: Reproductive Mode, Parental Care). The three
bers and sizes of eggs. Female Plethodon cinereus main- groups of amphibians have distinctive patterns and there-
tained on different feeding regimes for 6 months showed fore are treated separately.
a significant positive correlation between oocyte size and
maternal condition and between oocyte number and ini- Caecilians. Oviparous ichthyophiid caecilians may have
tial body weight (Fraser, 1980). There is evidence that a extended breeding seasons or even may be aseasonally
direct relationship exists between nutrition and oocyte reproductive in India and the Philippines, but data are
 Reproductive Strategies
inconclusive (M. Wake, 1977a). ¡chthyophis glutinosas ample, the aquatic P/eurode/es toa/tí has a prolonged 17
breeds only during the rainy season in Sri Lanka (Breck- breeding season through the warmer months. Annual
enridge and Jayasinghe, 1979). In the viviparous Der- cycles of reproduction are characteristic of the families of
mophis mexicanus in Guatemala, maüng occurs at the large, aquatic salamanders (Cryptobranchidae, Sireni-
beginning of the rainy season in May and June, and dae, Proteidae, Amphiumidae), and most of these repro-
gestation requires a full year; females have at least a duce in the spring. However, Amphiuma tridacfy/um re-
biennial cycle, but males have active spermatogenesis produces in the winter in Louisiana (Cagle, 1948); Siren
throughout most of the year (M. Wake, 1980b). These lacertina breeds in February and March in Alabama (Hanlin
limited observations emphasize the necessity to learn much and Mount, 1978); and Andrios dauidianus breeds in the
more about reproductíve cycles in caecilians. autumn in cold mountain streams in China (M. Chang,
1936).
Salamanders. Two major reproductíve patterns are In most salamanders exhibitíng annual seasonal repro-
exhibited by salamanders. The first, the classical annual duction, fertilizatíon is external (Cryptobranchidae, Hy-
pattern of aquatic breeders that begins in the spring, is nobiidae, Sirenidae), or oviposition occurs within a few
characterisüc of hynobiids, cryptobranchids, sirenids, am- hours to several days after mating (Ambystomatídae and
phiumids, proteiids, and most salamandrids and ambys- most Salamandridae). However, in some species mating
tomatids. Breeding activity is initíated primarily by the occurs in the autumn, and spermatozoa are stored in the
saturatíon of the ground by melüng snow and spring rains, spermatheca untíl the following spring. This pattern is
but temperature also is a factor, especially in aquatic spe- characteristic of Necturus (Bishop, 1926; Shoop, 1965b),
cies. Euproctus osper (Ahrenfeldt, 1960), Salamandra sala-
Within the annual pattems displayed by Ambystoma, mandra (Joly, 1960b), and various plethodontids.
it seems as though rising temperatures combined with The second major pattern is biennial reproduction and
saturatíon of the ground induce breeding migratíons and is characteristic of the terrestrial plethodontid salaman-
reproductive activity in those species that breed in the ders (Plethodontinae and Bolitoglossini). Species living
spring. Spring thaws are associated with breeding activity under similar climatic conditions usually have similar pat-
of various species of Ambystoma (Bishop, 1941; Baldauf, terns of activity and reproduction, but there are some
1952; Hassinger et al., 1970). For example, a combi- exceptions. The climatic conditions in the eastem and
nation of spring rains and temperatures of more than 10° western United States differ from one another and from
is necessary for spring migrations to breeding sites by conditions in Central America, and patterns of activity
Ambystoma in Tennessee (Gentry, 1968). However, and reproduction in plethodontid salamanders are dif-
springlike weather in midwinter can induce reproductive ferent in these regions (Fig. 2-1).
activity in A. tigrinum (Hassinger et al., 1970), so that In the seasonally températe climate of eastern United
subsequent low temperatures result in ice-covered ponds States, salamanders of the genera Aneides and Pletho-
in which both adults and eggs may be present. don are active at or near the surface of the ground from
The annual pattems of some other species of Ambys- spring until autumn. Mating usually occurs in late summer
toma are different because of the seasonal differences in or autumn and may occur again in the spring in the same
rainfall and temperatures throughout North America. populations. Oviposition takes place during a short span
Breeding activity is initiated by rainfall in coastal popu- of time in late spring or early summer. Females attend
lations of A. macrodacíy/um in California, but breeding their clutches of eggs for 2 or 3 months until hatching
in montane populations is associated with increased tem- occurs in late summer or early autumn. In those parts of
peratures (J. Anderson, 1967). In arid regions with mod- the western United States inhabited by plethodontid sal-
érate temperatures, rainfall is the primary factor inducing amanders (Aneides, Batrachoseps, Ensatina, Plethodon),
reproductive activity, as in A. rosaceum (J. Anderson, temperature is more equable than in the eastem part of
1961). Ambystoma annulatum, cingulatum, and opacum the country, but the dry summer months restrict the ac-
breed in the autumn (Noble and Marshall, 1929; Noble tivity of salamanders to autumn, winter, and spring; mat-
and Brady, 1933; J. Anderson and Williamson, 1976). ing occurs throughout the period of activity. With the
In Louisiana A. ta/poideum breeds in the winter, follow- exception of Batrachoseps, oviposition takes place during
ing a cooling trend in the modérate winter temperatures a brief period at the end of spring when salamanders
(Shoop, 1960). In some primarily aquatic species that retreat to subterranean refuges and attend their eggs dur-
live in cold streams—e.g., A. ordinarium (J. Anderson ing the inhospitable summer. In Guatemala, terrestrial
and Worthington, 1971) and fihyacotriton o/ympicus species of Bolitoglossa and Pseudoeurycea are active year-
(Nussbaum and Tait, 1977)—populations reproduce round. Spermatogenesis, and presumably mating, occurs
throughout the year, but Dicamptodon ensatus has sea- throughout the year. Oviposition takes place in Novem-
sonal reproduction (Nussbaum, 1969). ber at the beginning of the dry season, and females re-
Although annual breeding patterns, initiated by rising main with their clutches in subterranean retreats until the
temperatures and spring rains, are evident in most Eur- eggs hatch near the beginning of the rainy season. Spe-
asian salamandrids and hynobiids (Thom, 1968; Stew- cies of Bolitoglossa living in aseasonal high montane re-
ard, 1970), there are some notable exceptions. For ex- gions in the tropics show no seasonal patterns of activity,
LIFE HISTORY
18 Jul Qct cause of biennial cycles in Trituras alpestris (Joly, 1961);
both of these live at high elevations and presumably re-
Activity
quire two seasons in order to obtain sufflcient energy for
compleüon of oogénesis. Long periods of gestation—up
to 1 year in some montane populations of Salamandra
Courtship salamandra (Joly, 1961) and 2 to 4 years in S. aira
(V. Vilter and A. Vilter, 1960)—elimínate the possibility
of annual reproduction. In Amphiuma tñdacfylum, lengthy
^ Attends Eggs attendance of eggs, possibly resulting in malnourishment,
1 may be related to biennial cycles in some females (Cagle,
1948). Individuáis of some populations of species of Tar-
Jan _ Apr Jul _ Oct icha require long periods for migration to and from
breeding sites; in these populations both males and fe-
Activity iiíiiiSS^^i^íSi^iSSiiiiijiíiiií
males have biennial cycles (Twitty et al., 1964). Appar-
ently not all of the females in a population of Ambystoma
maculatum breed in any given year, a biennial or possibly
Courtship triennial cycle may exist (Husting, 1965).
Most plethodontíds having direct development of ter-
restrial eggs (plethodonünes and bolitoglossines) appar-
J Attends Eggs ently have biennial cycles in females (Houck, 1977b),
but Batrachoseps attenuatus has an annual cycle. Con-
siderable variation in, and/or interpretaüon of, data exists
Jan t Apr ( ^M Qct . in desmognathodontine and hemidactyline plethodon-
üds. Annual cycles have been hypothesized for Des-
Activity mognathus aeneus and some populations of D. fuscus,
Leurognathus marmoratus, Stereochilus marginatus,
Pseudotriíon ruber, and Gyrinophilus porphyriticus (see
Courtship Tilley, 1977, for references). Cycles seem to be irregular
in Pseudotriton montanus and in some populations of
Desmognathus ochrophaeus (Bruce, 1975; Tilley, 1977).
C; Attends Eggs
Biennial cycles have been suggested for five species of
Desmognathus in the southem Appalachian Mountains
(Organ, 1961). In most of the plethodontids with aquaüc
Figure 2-1. General patterns of surface activity, courtship, and larvae, courtship is most common in the autumn but also
egg attendance of terrestrial plethodontid salamanders in
A. eastern North America, B. western North America, and may occur in the spring; eggs usually are deposited in
C. Central America. The black bar indicates time when oviposition the summer. Annual oogenic cycles may be normal for
usually occurs; shading indicates time when activities usually some populations of Plethodon dnereus, glutinosus, and
occur. Modified from Houck (1977b).
wehrlei, although other populations of these species and
the majority of terrestrial plethodontids apparently have
matíng, or oviposition, such as B. adspersa (Valdivieso biennial cycles (Houck, 1977b; Tilley, 1977).
and Tamsitt, 1965) and B. subpalmata (Vial, 1968). Two factors contribute to apparent discrepancies in an-
Likewise, limited data suggest that B. peruana is acyclic nual versus biennial cycles. One is simply the method of
in an aseasonal lowland, tropical región (Duellman, 1978), sampling. The presence of gravid or brooding females
as is Dendrotriton brome/lacia, an arboreal species in sea- versus nonreproductive individuáis at the same time of
sonal forest in Guatemala (Houck, 1977b). year has been interpreted as evidence for nonannual pat-
Among the excepüons to tríese general patterns, Ba- terns, but such conclusions can be verified only by long-
trachoseps attenuatus and coastal populations of other term capture-recapture studies of marked individuáis.
species of Batrachoseps in California oviposit in the au- Second, evidence exists for geographic or altirudinal in-
tumn; courtship presumably occurs during the summer traspecific variation in patterns of life histories, including
when the salamanders are underground (Houck, 1977b). oogenic cycles. Furthermore, the situation is complicated
Pseudoeuycea rex inhabits higher elevaüons than the other by the existence of cryptic species. Southern populations
species of salamanders studied in Guatemala; its cycle is of Plethodon glutinosus have been reported to have an
reversed in comparison with the other species, that is, its annual cycle, and northern ones, biennial (Highton, 1962;
young hatch in November and December (Houck, 1977b). Organ, 1968), but now both cycles are known in the
Annual female reproductive cycles seem to be the rule north, and apparently two species exist there (R. High-
in the majority of non-plethodontid salamanders. How- ton, pers. comm.). Altirudinal differences in cycles have
ever, more lengthy cycles are known for some species. been found in Pseudotriton montanus, P. ruber, and
A short season of activify has been implicated as the Desmognathus ochrophaeus (Bruce, 1975, 1978b; Til-
 Reproductive Strategies
ley, 1977). Definitive evidence exists for altítudinal dif- tumn and spring) but to deposit only one clutch of eggs. 19
ferences in Salamandra salamandra (Joly, 1961); the In summary, most salamanders have definite seasonal
oogenic cycle is annual in lowland populations and bien- reproductíve cycles, which is expected of amphibians liv-
nial in montane populatíons (Fig. 2-2). ing in températe climates. Reproductíve actívity is in-
Under laboratory conditíons, Pleurodeles walti can de- duced by increasing spring temperatures, but mating may
posit eggs at intervals of 2 months (Gallien, 1952). A occur in the autumn in salamanders having internal fer-
captive female Triturus cristaíus mated twice and laid two tilization. The ability to store spermatozoa in the sper-
clutches of eggs in one season (Simms, 1968). Salaman- matheca over winter allows the delay of ovipositíon until
ders in nature apparentíy do not produce múltiple clutches the following spring. Rainfall also is essential for periods
in a given season or year. Individual témales are known of activity, especially in regions having equable temper-
to pick up spermatophores in successive seasons (au- atures throughout the year. Most species inhabiting re-
gions with seasonal rainfall oviposit and attend eggs in
subterranean refuges during the dry season. Biennial
oogenic cycles that seem to be associated with seasonal
temperature regimes and maternal care prevail in species
inhabiting aseasonal regimes on mountains in the tropics.

Anurans. Among anurans, two basic reproductíve pat-

terns are evident. Most tropical and subtropical species
are capable of reproductíon throughout the year; rainfall
seems to be the primary extrinsic factor controlling the
timing of reproductíve actívity. In most températe species,
reproductíve actívity is cyclic and dependent on a com-
binatíon of temperature and rainfall.
In aseasonal, wet, tropical lowlands both sexes are re-
productive throughout the year. This has been demon-
J M M S N J M M J S N strated for several species in tropical Asia and Indonesia
Figure 2-2. Female sexual cycle of Salamandra salamandra from (Hing, 1959; Church, 1960a, b; Inger and Greenberg,
Sarthe In western France, elevation 70 m (lower graph) and from 1963; Berry, 1964; Inger and Bacon, 1968) and in the
Cauterets in the Pyrenees, 1000 m (upper graph). Lines show a upper Amazon Basin in South America (Crump, 1974;
2-year cycle of weight of left ovary as percent of total weight. Bars
indícate periods of gestaton. O = oviposition; P = parturition. Duellman, 1978). In tropical Oriental species of ñaña and
Redrawn from Joly (1961). Bufo that have been studied, both male and female cycles

65

-55
33
200 O)
'

-45 ^
o Figure 2-3. Continuous reproductíve
3 cycle of Rana erythraea and climatic
variation at Kuching, Sarawak,
35 Borneo. Thickness of nuptial
excrescences and humeral glands
measured in micrometers.
A. Humeral glands in males.
25 B. Nuptial pad glands. C. Nuptial
pad epithelium (broken lines indícate
absence of data in October and
December). D. Percent of témales
with matare ova. The range of
máximum and mínimum
temperatures is shaded; monthly
rainfall is indicated by the dotted
O N D J F M M June Une. Data are for 1 year beginning in
Jury 1957, as given by Inger and
Months Greenberg (1963).
LIFE HISTORY
are continuóos (Fig. 2-3). In the upper Amazon Basin,
•1977
rainfall occurs throughout the year but is uneven and 1978
unpredictable; four patterns are evident among the 87 30
species of anurans in one área in Amazonian Ecuador:
1. Continuous—Breed essentially every night with = 2CH
the exception of clear, dry nights with intense CD

moonlight.
2. Opportunistic—Breed regularly after heavy rains 10
throughout the year.
3. Sporadic wet—Breed sporadically after heavy
rains.
o
4. Sporadic dry—Breed sporadically during infre- J F M A M J J A S O N D
quent dry periods. Months

Presumably all of the species in that área are physio- Figure 2-4. Rainfall and reproductive season (horizontal bars) of
logically capable of reproduction throughout the year, Hyla rosenbergi during 2 successive years in a seasonally rainy site
in central Panamá. Modified from Kluge (1981).
but availability of breeding sites may limit the contínuity
of reproductive activity in many species. Those frogs that
oviposit in ephemeral aquatic sites are dependen! upon rainfall (B. Balinsky, 1969); the exception, Bufo regularía,
heavy rains; those that utilize streams usually breed at breeds in streams. Spadefoot toads, Scaphiopus, breed
times of little rainfall, when the water level is low and the only after heavy rains that completely soak the ground
current is slow. Thus, even though temperature and and form temporary pools, and when temperatures are
moisture may be sufficient throughout the year, unpre- above 11° (Bragg, 1945; Hansen, 1958). Likewise, the
dictability of oviposition sites probably restricts reproduc- burrowing Cyclorana platycephala breeds only after rains
tive activity. in the spring and summer but not in the winter (van
In the seasonably dry tropics, anuran reproductive ac- Beurden, 1979). In this species, gametogenesis is contin-
tivity is closely associated with the rainy season. Analysis uous throughout the year but reduced in winter; some
of breeding patterns of 13 species of anurans breeding females retain eggs over winter. Thus, in arid regions,
in a pond in the llanos of Venezuela revealed a cióse anurans are primarily opportunistic breeders with the ad-
correlation between breeding activity and the rainy sea- vent of sufficient rainfall at times of adequate tempera-
son in 1974 and 1975, when the pronounced dry season tures.
occurred from January to May, but in 1976, when some Eurasian discoglossids exhibit a pattem of múltiple
rain fell during the dry season, breeding activity by some breedings during the warm season of the year; Alytes,
species was more or less continuous (Hoogmoed and Bombina, and Discog/ossus have two to six clutches per
Gorzula, 1979). These observations suggest that the frogs season (Knoepffler, 1962; Obert, 1977; Crespo, 1979).
are capable of continuous reproduction, even though cli- Reproduction is phased in periods of 2-4 weeks in the
matic conditions restrict their reproductive activity tem- spring and summer, after which gametogenesis termi-
porally. Similarly, reproductive activity associated with nates in Alytes and Bombina. However, gametogenesis
rainfall is evident in two species of Ptychaderta in West and reproduction are potentially continuous in Discog-
África (Barbault and Trefaut Rodrigues, 1978) and in íossus picíus; individuáis maintained in the laboratory de-
Hyla rosenbergi in central Panamá (Kluge, 1981) posited up to 10 clutches per year (Knoepffler, 1962).
(Fig. 2-4). Although températe anurans respond to rainfall, tem-
The development of mature eggs and male secondary perature seems to be a major factor initiating breeding
sexual characters may precede the breeding season in activity, as evidenced by geographic variation in the time
some seasonal breeders; thus, such species seem to be of breeding. fíana sylvatica breeds in January and early
cyclic in their innate reproductive features as well as their February in Georgia and North Carolina (Martof and R.
breeding activity. For example, at Upemba in West Áf- Humphries, 1959) but not until April-June in the north-
rica, where there are sharply defined wet and dry sea- ern part of its range (Herreid and Kinney, 1967). Like-
sons, males of 12 species are cyclic, and 6 are acyclic, wise, Scaphiopus holbrooki and Hyla crucifer breed at
but females of only 4 of the 18 species are acyclic times of winter rains in Florida but not until spring or
(K. Schmidt and Inger, 1959). Cyclic nature of breeding summer in New England and Canadá (A. F. Carr, 1940;
associated with rainfall is evident in Australian myoba- Logier, 1952; Hansen, 1958). Breeding seasons may be
trachids of the genus Heleioporus (A. Lee, 1967). 5 or 6 months long in southern températe frogs, whereas
In subtropical and températe regions characterized by in the north the season may be restricted to 1 or 2 weeks
seasonal rainfall, breeding activity is initiated by rainfall. (Einem and Obert, 1956; W. Blair, 1961; Herreid and
In the vicinity of Johannesburg, South África, the breed- Kinney, 1967; L. Licht, 1969). Similar patterns of earlier
ing activity of all but one species is closely associated with versus later breeding seasons are associated with altitude,
 Reproductive Strategies
as evidence by coastal versus tnontane populations of Two clutches per breeding season are known for some 21
Rana pretiosa (F. Turner, 1958; L Licht, 1969) and prai- températe species: Hyla chrysoscelis (S. M. Roble, pers.
rie versus montane populations of Pseudacrís tríseríata comm.), Pseudacris triseriata (S. M. Roble, pers. comm.),
(Pettus and Angleton, 1967). At high latitudes, as well as Rana c/am¡tans (Wells, 1976), R. caíesbeiana (R. W.
at high altitudes in températe regions, breeding seasons Howard, 1978), Bu/o valliceps (W. Blair, 1960), and
are greatly restricted by temperature, as noted in Bu/o B. looodhousii (Thornton, 1960). Rana sphenocephala
variegatus and Pleurodema bufonina in southem Argen- in central Texas deposits three clutches per year (D. M.
tina and Chile (Cei, 1961; Hock, 1967). Hillis, pers. comm.). Most female Hyla cinérea, gratiosa,
A combination of a certain amount of rainfall at or and regula breed only once per season, but some indi-
above a certain temperature is known to be responsible viduáis have two clutches, and 5 of 248 H. cinérea fe-
for breeding activity in some températe species— Bu/o males and 3 of 85 H. regula females had three clutches
bu/o (Heusser, 1960), B. valliceps (W. Blair, 1960), and in one season (Perrill and R. Daniel, 1983). The múltiple
Rana aurora (Storm, 1960). clutches of discoglossids have been mentioned already.
Other factors stimulating reproducüon include differ- Individuáis in some populations of Bu/o may repro-
ences in Ijght intensity over short periods of time in some duce biennially (Bragg, 1940; A. Blair, 1943); females of
pipids—Hymenochirus boettgerí (G. Rabb and M. Rabb, Rana pretiosa in the Rocky Mountains in Wyoming re-
1963a) and Xenopus laeuis (R. Savage, 1965). Savage produce every second or third year (F. Turner, 1960),
also demonstrated experimentally that a water-soluble and in some populations of Ascaphus truei females de-
substance associated with algae stimulated spawning in posit eggs in altérnate years (Metter, 1964a).
Rana temporaria. No consistent effects of temperature, In summary, anurans in tropical and subtropical en-
rainfall, humidity, or light can be correlated with dates of viroments tend to have continuous reproductive cycles
breeding of that species in England (R. Savage, 1961); and breed throughout that part of the year when rainfall
presumably the frogs respond to odors produced by al- is sufficient to provide oviposition sites. Individuáis may
gae, the growth of which is influenced by rainfall in the breed many times during a season; females of some spe-
previous month. cies can produce clutches only 2 weeks apart. At higher
Although it is known that populations of tropical anu- elevations and at higher latitudes, temperature becomes
rans breed throughout the year, the frequency of repro- an important factor in the reproductive patterns, con-
ducüon by individual females is poorly known. Hyla ro- trolling time of breeding and length of breeding season.
senbergi (Kluge, 1981) and Smi/isca cyanosticta (Pyburn, Annual reproduction by females is most common in tem-
1961) produce as many as six clutches in a single breed- pérate regions, but individual females in some popula-
ing season. Phyllomedusa trinttatus in Trinidad (Kenny, tions deposit two or more clutches in a single season,
1966) and Syrrhophus mamocki in Texas (Jameson, whereas in populations existing in extremely cold envi-
1955a) produce three clutches during a season. Two ronments females may not produce eggs every year.
clutches were produced a month apart by Hyla rhodo-
pepla (Crump, 1974), and some female Bu/o typhonius
produced two clutches in 6 weeks (Wells, 1979). Fre- REPRODUCTIVE MODE
quency of breeding by captive individuáis has been re- Mode of reproduction as used by Salthe (1969) and Salthe
ported for several species: Hyperotius viridiflavus repro- and Duellman (1973) is a combination of ovipositional
duced at intervals of 2-3 weeks for a year (Richards, and developmental factors, including oviposition site, ovum
1977); Eleutherodactylus johnstonei reproduced every and clutch characteristics, rate and duration of develop-
2-3 months (Chibon, 1962); Dendrobates auratus pro- ment, stage and size of hatchling, and type of parental
duced 10 clutches in 170 days (Senfft, 1936); Phy//o- care, if any.
bates uittaíus produced clutches at 2-week intervals (Sil- The diversity of reproductive modes in amphibians is
verstone, 1976); Pipa carvalhoi produced clutches 4—8 much greater than that observed in other groups of ver-
weeks apart (Weygoldt, 1976a); Pipa pama produced tebrates, especially the amniotes. In each of the three
three or four clutches per year (Sughrue, 1969). Lim- living orders of Amphibia there are trends toward terres-
nodynostes tasmaniensis may deposit clutches at 2-week triality. The variety of these trends is especially note-
intervals throughout the year (Tyler, 1976). Probably worthy in anurans. These reproductive adaptations have
múltiple clutches are the rule among tropical anurans in been viewed as pioneering evolutionary experiments in
nature, but a lengthy breeding season is not necessarily the conquest of terrestrial environments by vertebrates
indicativo of many clutches per female; for example, al- (C. Goin, 1960). Especially important is the evolution of
though Colostethus inguinalis has a lengthy breeding direct development of terrestrial eggs, ovoviviparity, and
season, females deposit only two clutches per season viviparity that have been important in the successful in-
(Wells, 1980a). On the other hand, in the Ecuadorian vasión of montane enviroments by amphibians.
Andes, brooding marsupial frogs, Gastrotheca riobam- The diversity of reproductive modes is quite different
bae, can be found throughout the year, but individual in the three living groups of amphibians. Therefore, the
females produce only one clutch per year (del Pino, 1980). groups are treated individually.
LIFE HISTORY
Caecilians the Hynobiidae, Cryptobranchidae, and presumably the
All caecilians are known, or presumed, to have internal Sirenidae. Mating has not been observed in sirenids, but
fertilization; probably about 75% of the species bear liv- the absence of a spermatheca in females and cloacal
ing young (M. Wake, 1977a, 1977b). A major dichotomy glands in males seems to preclude the production of sper-
in caecilian reproducüve modes is that of oviparity versus matophore, the only known method of intemal fertiliza-
viviparity. Among oviparous caecilians, ichthyophüds and tion in salamanders. External fertilization seems likely in
probably rhinatremattds have terrestrial eggs adjacent to Siren, which deposits eggs in clumps in water, but un-
water; both families are characterized by aquatic larvae, reasonable in Pseudobranchus, which scatters its eggs
as exemplified by Caudacaecilia weberi, Ichthyophis glu- singly among aquatic vegetation (Goin et al., 1978). The
tinosus, and Epicrionops petersi. Oviparity also occurs in spermatozoa of Pseudobranchus striatus are large and
members of the Caeciliidae; in some caeciliids (e.g., Geo- highly motile, perhaps to facilítate the fertilization of scat-
trypetes grandisonae and three species of Grandisonia,) tered eggs (Austin and C. Baker, 1964). The eggs of
aquaüc larvae are known, whereas in others (e.g., Gran- cryptobranchids are unpigmented and deposited in pairs
disonia brevis and G. diminutiva, Hypogeophis rostratas, of strings under rocks in streams; the pigmented eggs of
Idiocranium russeli, and, presumably, Gegeneophis and hynobiids are deposited as pairs of elliptical sacs, one
Uraeotyphlus) the terrestrial eggs undergo direct devel- from each ovary, in ponds or streams. In these families,
opment, and there is no aquatic larval stage. sperm are released by the males after the eggs are de-
Members of the aquatic family Typhlonectidae are vi- posited. An exception is the hynobiid Ranodon sibiricus,
viparous and produce aquatic larvae. Viviparity and the males of which produce spermatophores; however, fer-
absence of aquatic larvae are characteristic of many Oíd tilization is external, for females apparently deposit egg
World species of caeciliids (e.g., Geotrypetes angelí and sacs on top of the spermatophores (Bannikov, 1958).
G. seraphini, Schistometopum thomense, and Sco/eco- Internal fertilization exists in about 90% of the species
morphus uluguruensis) and New World genera (e.g., of salamanders. Among these, aquatic eggs and larvae
Dermop/iis and Gymnopisj. are characteristic of all proteiids and amphiumids, most
Although the mode of reproduction is not known for ambystomatids, nearly all salamandrids, and aquatic
many genera and species of caecilians, an evolutionary plethodontids. Terrestrial eggs are deposited in depres-
pattern does seem to be emerging. The mode of primitive sions by Ambystoma cingulatum and A. opacum; with
families (Ichthyophiidae and Rhinatrematidae), that is, the advent of rains the depressions fill with water and the
oviparity with aquatic larvae, also occurs in a few mem- eggs hatch into-aquatic larvae. Two plethodontids, Hem-
bers of the Caeciliidae. In that probably composite family idactylium scutatum and Stereochilus marginatus, have
there is a trend toward increasing terrestriality through terrestrial nests in sphagnum moss or rotting wood; upon
oviparity and direct development to viviparity. The di- hatching, the larvae wriggle into the water below the nest.
vergent, aquatic typhlonectids are viviparous with aquatic Other salamanders having terrestrial eggs lack an aquatic
larvae. larval stage. In one of these, Desmognathus aeneus, the
eggs hatch into nonfeeding larvae that complete their
Salamanders development in the nest (J. Harrison, 1967). The eggs
The three modes of reproduction in salamanders defined of plethodontine and bolitoglossine plethodontids have
by Salthe (1969) are based primarily on oviposition site direct development.
and do not take into consideratíon other factors incor- Eggs are retained in the oviducts in four species of
porated into the concept of reproductive mode. The ma- salamandrids. Under normal conditions, lowland popu-
jor dichotomy in salamander reproduction is external ver- lations of Salamandra salamandra and Mertensiella cau-
sus intemal fertilization by means of a spermatophore. cásica have aquatic larvae, but montane populations of
Six reproductive modes can be recognized among sala- the former and gravid females of the lafter subjected to
manders having internal fertilization. The seven modes prolonged drought retain the eggs and eventually give
are outlined as follows: birth to either larvae or fully developed young (Muskhel-
ishvili, 1964; Joly, 1971; Fachbach, 1976). Salamandra
I. Fertilization external; eggs and larvae aquatic atra and Mertensiella luschani antalyana are viviparous
II. Fertílizatíon intemal (Hafeli, 1971; Ózeti, 1979).
A. Eggs and larvae aquatic External fertilization unquestionably is primitive in sal-
B. Eggs terrestrial; larvae aquatic amanders. The evolution of intemal fertilization probably
C. Eggs terrestrial; larvae terrestrial, nonfeed- occurred only once in salamanders and was a precursor
ing to direct development, which evolved independently in
D. Eggs terrestrial; direct development salamandrids and in different phyletic lines in plethodon-
E. Eggs retained in oviducts tids. The trend from aquatic eggs and larvae to direct
1. Ovoviviparous development of terrestrial eggs is illustrated well by des-
2. Viviparous mognathine plethodontids in the southem Appalachian
Mountains (Table 2-1), as first pointed out by E. Dunn
External fertilization of aquatic eggs is characteristic of (1926a) and srudied by Organ (1961). The fossorial
 Reproductive Strategies
Table 2-1. Teirestrial Trends in Desmognathine Salamanders 23
Speciec Esa» Larvae Adults
Leurognathus marmoratus Large streams Large streams Large streams
Desmognathus quadramaculatus Streams and seeps Small streams Small streams and seeps
Desmognathus montícola Streams and banks Small streams Small streams and seeps
Desmognathus fuscus Stream banks and seeps Headwaters of small Headwaters of small
streams streams and seeps
Desmognathus ochrophaeus Stream banks and seeps Streams and seeps Terrestrial
Desmognathus aeneus Seepage áreas Terrestrial Terrestrial
Desmognathus wrighti Seepage áreas Direct development Terrestrial
Phaeognathus hubrichti Moist soil Direct development Terrestrial

Phaeognathus hubrichti presumably has direct develop- feeding larvae (Mode 4) is known in only a few species:
ment of terrestrial eggs. the bufonids Dendrophryniscus brevipollicatus (Car-
valho, 1949) and Mertensophryne micranotus (Grandi-
Anurans son, 1980b); and the hylids Aparasphenodon brunoi and
In contrast to salamanders and caecilians, practically all Hyla perpusilla (Lutz, 1954), Phrynohyos resinifictrix (B.
anurans have externa! fertílization; in fact, internal ferül- Zimmerman and Hodl, 1983), Phyllodytes (Bokermann,
ization is known only in Ascaphus, the species of Necto- 1966a), Anotheca spinosa and members of \heHyla bro-
phrynoides, Mertensophryne micranotis (Grandison and me/iacia group (Duellman, 1970), and Jamaican Hyla
Ashe, 1983), and two species of Eleutherodactylus and Calyptahyla crucialis (E. Dunn, 1926a).
(Townsend et al., 1981), but internal ferülizatíon may be An independen! preadaptation for direct development
more widespread in Eleutherodactylus and other frogs is seen in the Ufe histories of frogs that produce eggs with
having terrestrial eggs. However, within the constraints sufficient yolk to provide nourishment for the developing
of externa! fertilization, anurans have a great diversity of tadpoles after they hatch from aquatic eggs (Mode 5).
reproductive modes. Three major categories defined on The only known examples of this mode are the lepto-
the basis of the site of egg development contain 29 modes dactylids Eupsophus roseus and E. vitíatus in southem
(Table 2-2). Modes 7, 10-11, 14, 16, and 24-27 are Chile (Formas and Vera, 1980) and the Philippine bu-
associated enürely with obligatory párenla! care and are fonids Pelophryne albotaeniata and P. lighti (Inger, 1954),
discussed in the following sectíon. The others, discussed in which eggs and nonfeeding tadpoles develop in water-
here, are referenced by the numbers in Table 2-2. fllled depressions in the ground. Similarly, complete de-
The most common and phylogenetically widespread velopment of aquatic eggs and nonfeeding tadpoles in
(15 of 21 families) site of oviposition is in free water— water-fllled cavities in trees or axils of leaves (Mode 6) is
standing (Mode 1) or flowing (Mode 2), permanent or known in three genera of Madagascaran microhylids: An-
temporary. Aquatic eggs and tadpoles are characteristic odonthyla, Platypelis, and Plethodontohyla (Blommers-
of all ascaphids, rhinophrynids, Oíd World pipids, pelo- Schlósser, 1975b). Likewise, eggs and nonfeeding tad-
batíds, pelodytids, pseudids, and most discoglossids, bu- poles of the Bornean microhylid Ka/ophrynus pleuro-
fonids, hylids, and ranids; they also occur in some groups stigma develop in water-filled cavities in logs (Inger, 1966).
of myobatrachids, leptodactylids, microhylids, hypero- The construction of a foam nest on the surface of the
liids, and rhacophorids. Eggs and feeding larvae in quiet water in ponds (Mode 8) or streams (Mode 9) is char-
water are characteristic of such diverse frog genera as acteristic of many limnodynastine myobatrachids and most
Xenopus, Pelobates, Bufo, Hyla, Rana, and Gastro- leptodactyline leptodactylids (A. Martín, 1970). The
phryne. Similarly, in lotic sites (streams), the diversity is Chínese rhacophorid Chiñxalus nongkhorensís also has
great, including genera such as Ascaphus, Scutiger, Ate- foam nests on the surface of ponds (Liu, 1950). Only the
lopus, Plectrohyla, Buergeria, as well as some Rana and Australian Megisto/otis lignarius places foam nests in pools
Hyla. The flowing and quiet water modes are recognized that become rapidly flowing streams after rains (Tyler
as different principally because of the adaptations of the et al., 1979). " j
tadpoles (see Chapter 6). The deposition of eggs out of water is a major step in
The habit of depositing eggs as a surface film in a the trend toward terrestriality in anurans. In some species,
shallow natural basin or one excavated by the male (Mode the eggs are deposited in a terrestrial nest near water; the
3) is known only in a few Neotropical Hyla—H. vasta eggs hatch when the nest floods, and the tadpoles feed
(Noble, 1927a) and members of the H. boans group and develop in ponds or streams (Mode 12). This mode
(Kluge, 1981). Ovarían and early larval development oc- is known in the Asian Rana adenop/eura (Liu, 1950) and
cur in the basin; subsequent flooding results in the tad- in species of the myobatrachid genera Geocrinia (Watson
poles dispersing into open water. and A. Martin, 1973) and Pseudophryne (Woodruff,
The utílizatíon of water trapped in cavities in trees or 1976a).
in the axils of bromeliads for development of eggs and Various kinds of frogs deposit their eggs on land, rocks,
LIFE HISTORY
or tree roots near water, or even in burrows; when the families: Sooglossidae— Sooglossus gardinerii (Nuss-
tadpoles hatch they wriggle to, or drop into, the water baum, pers. comm.), Myobatrachidae— Arenophryne
and begin their feeding existence (Mode 13). Eggs are rotunda (Roberts, 1984), Geocrinia rosea (Watson and
deposited on rocks or roots above streams, into which A. Martin, 1973), and Myobatrachus gouldii (Roberts,
hatchlings drop, in the species of the Australian Mixo- 1981), and Rhacophoridae—three species of Philautus
phyes (Watson and A. Martin, 1973), in Centro/ene gec- (W. Brown and Alcalá, 1983), and Rhacophorus micro-
koideum (J. D. Lynch et al., 1983), Rana magna (Alcalá, tympanum (Kirüsinghe, 1957). Also, this mode is known
1962), and the African ranid Natalobatrachus bonebergi in one Neotropical microhylid, Myersiella microps (Izeck-
(Wager, 1965). Chilean leptodactylids of the genus Ba- sohn et al., 1971), and probably also occurs in Syncope,
trachyla placa their eggs out of water near streams or as well as the Neotropical bufonids Oreophrynella, Osor-
pools, and the natchling tadpoles either drop into or wrig- nophryne, and Rhamphophryne. Eggs undergoing direct
gle to the water (Formas, 1976a). Some hyperoliids of development on vegetatíon (Mode 20) are not common
the genus Leptopelis deposit eggs in soil near water in Eíeutherodactylus (usually in bromeliads but some-
(SchLatz, 1963); upon hatching, the tadpoles wriggle to tímes on leaves) and are characteristic of the arboreal
the surface and then to water (Oldham, 1977). African species of the southern Pacific ranid genus P/atymaníis
Hemísus deposit eggs in subterranean nests attended by (W. Brown, 1952; Alcalá, 1962).
the females; when the eggs hatch, the female burrows to Many kinds of arboreal frogs deposit eggs above water,
water, which may be as far as 1 m away from the nest, into which hatchling tadpoles drop. In most of these the
and the tadpoles wriggle to water to begin feeding (Wager, tadpoles develop in ponds or streams (Mode 18). Those
1965). that develop in ponds include most of the phyllomedu-
The terrestrial eggs of some anurans hatch into non- sine hylids and members of the Hyla leucophyllata group
feeding tadpoles that complete their development in the (Duellman, 1970), plus most of the African Hyperolius
nest, with nutrition provided by the yolk (Mode 15). This (Drewes, 1984) and the Madagascaran ranids of the ge-
mode is known in two species in South America—the nus Mantidacty/us (Blommers-Schlosser, 1979a). Eggs on
leptodactylid Thoropa lutzi (Bokermann, 1965b) and the vegetaüon above streams are characteristic of the Cen-
microhylid Synapturanus safeeri (Pybum, 1975)—and four trolenidae (except Centro/ene^ and for various hylids—
African species—the bufonid Nectophrynoides malcolmi Phyllomedusa gutíata group (Bokermann, 1966a), Li-
(Grandison, 1978) and the ranids Phrynodon sandersoni toria iris (Tyler, 1963b), and Hyla /encasten and H. tho-
(Amiet, 1981), Arthroleptella hewitti and A. lightfooti rectes (Duellman, 1970). Rana /eytensis in the Philip-
(Wager, 1965). Addiüonally, terrestrial eggs or tadpoles pines is reported to deposit eggs in strings coiled on leaves
that hatch from terrestrial eggs are carried by adults (Modes above streams, but more frequently on moss-covered
14, 16, 24-27) (see the following section: Parental Care). roots or rocks (Alcalá, 1962). Some Oíd World tree frogs
Direct development of terrestrial eggs (Mode 17) is adhere their eggs to walls of caviües in trees; the hatchling
common among frogs inhabiting perpetually humid re- tadpoles drop into water in the cavity, where they feed
gions, as well as some drier áreas, and occurs in eight or and complete their development (Mode 19). This mode
nine families. Reproductíon in the Leiopelmatidae has been reported only in the African hyperoliid
(B. Bell, 1978) is limited to direct development of ter- Acan£hixa/us spinosus (Perret, 1962) and three Oriental
restrial eggs. The large, unpigmented ovarían eggs and rhacophorids, Theloderma stellatum (Liu, 1950), Nyctix-
terrestrial habits of the adults strongly suggest direct de- alus pictus (Inger, 1966), and N. spinosus (W. Brown
velopment of terrestrial eggs in the two genera of the and Alcalá, 1983).
Brachycephalidae (Izecksohn, 1971). This mode is char- Terrestrial íoam nests are known in three families. Some
acteristic of the immense leptodactylid genus Eleuthero- frogs construct nests in burrows or depressions that sub-
dactylus, related genera composing the tribe Eleuthero- sequently flood, and feeding larvae escape into ponds
dactylini (J. D. Lynch, 1971), and Australo-Papuan or streams (Mode 21). This is the mode known in the
microhylids of the subfamilies Asterophryinae and Gen- myobatrachid genus Heleioponts (A. Lee, 1967), the
yophryninae (Zweifel, 1972a). Thus, in the leptodactylids Leptodactylus fuscus group (Heyer, 1969), and some
and Australo-Papuan microhylids alone, direct develop- Asiatic rhacophorids— Polypedates bambusicola (Liu,
ment presumably occurs in more than 500 species. In 1950) and Rhacophorus schlegeli schlegeli (Okada, 1966).
additíon, this is the mode of development in African ran- In others, nonfeeding tadpoles complete their develop-
ids of at least some species of the genera Arthroleptis and ment in terrestrial foam nests (Mode 22). This is known
Anhydrophryne (Lamotte and Perret, 1963; Wager, 1965), in the myobatrachids Kyarranus (Moore, 1961) and Phi-
reported for Rana hascheana in Thailand (E. Taylor, 1962), loria (Littlejohn, 1963) and in the leptodactylids of the
and known or presumed on the basis of large, unpig- genus Adenomera (Heyer and Silverstone, 1969) and
mented eggs in the ranid genera Batrachylodes, Cera- Leptodactylus fallax (Lescure, 1979). Various Oíd World
tobatrachus, Discodeles, Palmatorappia, and P/atymaníis tree frogs have foam nests in trees and bushes over ponds
in the Salomón Islands (W. Brown, 1952). Direct devel- or streams, into which the tadpoles drop, usually soon
opment of terrestrial eggs occurs in at least three other after hatching. These include Asiatic rhacophorids, such
 Reproductive Strategies
as Philautus hosii (Inger, 1966), various species of Po- cavities adjacent to water in the L. pentadactylus group,
fypedates (C. Pope, 1931; Liu, 1950; Alcalá, 1962), and and placed in a burrow on land in the L. fuscus group.
Rhacophorus (Siedlecke, 1909; Alcalá, 1962; Okada, Aquatic larvae are present in all of these groups. The
1966). Arboreal foam nests over ponds are well known derived genus Adenomera has nests in a terrestrial cham-
in the African rhacophorid genus Chiromantis (Wager, ' ber, and the nonfeeding tadpoles complete their devel-
1965; Coe, 1974) and also have been reported for the opment in the nests. Within this series of adaptive types
hyperoliid Opisthothylax immaculatus (Amiet, 1974). toward increased terrestriality, there is a trend for an in-
The retenüon of eggs in the oviducts is known in only crease in the size of the ova and a decrease in the number
five species of frogs (M. Wake, 1978, 1980a). In three of eggs.
of these— Eleutherodactylus jasperí, Nectophrynoides Foam nests provide protection against desiccation; the
tomieri, and N. vivíparas —the eggs complete their de- upper surface exposed to air becomes viscous and even
velopment with nutrition provided only by the yolk; henee, dries to form a thin crust, while the interior remains moist.
they are ovoviviparous (Mode 28). However, in N. lib- In ephemeral ponds, in which water level fluctuates, many
eriensis and N. occidentalis true viviparity (Mode 29) oc- nests may be out of water for a day or two; the interior
curs; maternal nutrition is provided to the developing of the nest remains moist, and even recently hatched
young by oviducal secretions. Ovoviparity or even vivi- tadpoles may remain in the nest for a day or two until
parity may be more common than is realized among frogs. the water level rises. Nests subjected to these conditions
The discovery of ovoviparity in one of the more than 400 are present not only in the Leptodactylus melanonotus
species of Eleutherodactylus indicates the possibility that and L. ocellatus groups, but also in Paludicola, Physa-
other species of this genus, as well as others that are laemus, and Pleurodema. Construction of a foam nest in
thought to be oviparous, might produce living young, as an underground chamber, as exhibited by members of
suspected long ago in another species, E. orcutti, in Jamaica the L. fuscus group, coincides with the first heavy rains
(Lynn and C. Grant, 1940). Furthermore, at least one of the seascn. Subsequent heavy rains cause a rise in
oviparous species, E. coqui, has intemal fertilization water level and flood the nest, and the tadpoles escape
(Townsend et al., 1981). from the chamber. Tadpoles of L. bufonius may remain
It is generally conceded that Mode 1 (lentic eggs and in the foam nest for up to 39 days after hatching; during
tadpoles) is not only the generalized but also the primitive this time they do not feed and actually may decrease in
mode of reproduction in anurans. Assuming this to be size (Philibosian et al., 1974). Experimental evidence
true, there are diverse grades of specializaüon that can suggests that some biological property of the foam inhib-
be associated with an adapüve radiation into various en- its the rate of growth (Pisano and del Río, 1968). Fur-
vironments— ephemeral aquatic situaüons, some of which thermore, tadpoles of L. bufonius are ureotelic (Shoe-
are predictably present only during a brief rainy season, maker and McClanahan, 1973); therefore, wastes can
and streams, which allow anurans to escape from the accumulate in the nest chamber without being toxic to
constraints of lentic waters characteristic of lowlands. Other the tadpoles. All of these attributes are beneficia! to pro-
trends involve terrestrial eggs with subsequent larval de- longed survival in foam in the nest chamber.
velopment taking place in water. These trends have been Foam nests floating on open water or in water-filled
carried further in some groups—to the development of depressions are subject to intense sunlight. Comparisons
larvae on land, to direct development, and to ovovivi- of temperatures within nests and of shallow, water-filled
parity in a few species and eventually viviparity in two depressions show that the nests are about 5°C cooler
species (Fig. 2-5). than the water in the depressions and closely approxi-
Trends toward terrestriality result in the production of mate the temperatures of diurnal retreats of the frogs
larger-yolked eggs, accompanied by a reduction in the (Gorzula, 1977). Thus, a variety of ecological, develop-
number of eggs by anurans of similar size (Salthe and mental, and physiological evidence points to the foam
Duellman, 1973). Increasingly larger yolk reserves are nests of leptodactylids as an adaptation to seasonally wet
necessary for placing more advanced (proportionately environments with high temperatures and fluctuating water
larger) offspring in the environment. This trend is illus- levéis. On the other hand, terrestrial foam nests in which
trated well by comparison of ovum sizes in the sequenüal the tadpoles complete their development (Adenomera)
series of those that have aquatic eggs in lentic water, are characteristic of humid tropical forests.
aquatic eggs in lotic water, terrestrial eggs with aquatic Limnodynastine myobatrachids of Australia show a trend
larvae, terrestrial eggs with terrestrial larvae or direct de- in foam nesting and development similar to that of the
velopment (see following secüon: Quantitattve Aspects: Neotropical leptodactylines (A. Martin, 1970). Again, the
Fecundity). generalized foam nest floats on open water, as in Lim-
Reproductive modes associated with the construcüon nodynostes, Lechriodus, and Adelotus; frogs in these
of foam nests in the Leptodactylinae provide an excellent genera have numerous small eggs and aquatic larvae.
example of the trend toward terrestriality (Heyer, 1969). Limnodynostes interioris constructs nests in water-filled
The nest is on the top of open water in the Leptodactylus burrows in the banks of streams, and the species of Hel-
melanonotus and L. ocellatus groups, placed in water in eioporus place nests in dry burrows that subsequently
LIFE HISTORY
na
•*" Table 2-2. Outline of Reproducüve Modes in Anurans

I. Eggs aquatic
A. Eggs depositad in water
1. Eggs and feeding tadpoles in lentic water
2. Eggs and feeding tadpoles in lotic water
3. Eggs and early larval stages in natural or constructed basins; subsequent to flooding,
feeding tadpoles in ponds or streams
4. Eggs and feeding tadpoles in water in tree boles or aerial plants
5. Eggs and nonfeeding tadpoles in water-fllled depressions
6. Eggs and nonfeeding tadpoles in water in tree holes or aerial plants
7. Eggs deposited in stream and swallowed by female; eggs and tadpoles complete
development in stomach*
B. Eggs in foam nest
8. Foam nest on pond; feeding tadpoles in pond
9. Foam nest in pool and feeding tadpoles in stream
C. Eggs imbedded in dorsum of aquatic female
10. Eggs hatch into feeding tadpoles in ponds
11. Eggs hatch into froglets
II. Eggs terrestrial or arboreal
D. Eggs on ground or in burrows
12. Eggs and early tadpoles in excavated nest; subsequent to flooding, feeding tadpoles in
ponds or streams
13. Eggs on ground or rock above water or in depression or excavated nest; upon hatching,
feeding tadpoles move to water
14. Eggs hatch into feeding tadpoles that are carried to water by adult
15. Eggs hatch into nonfeeding tadpoles that complete their development in nest
16. Eggs hatch into nonfeeding tadpoles that complete their development on dorsum or in
pouches of adult
17. Eggs hatch into froglets
E. Eggs arboreal
18. Eggs hatch into tadpoles that drop into ponds or streams
19. Eggs hatch into tadpoles that drop into water-filled cavitíes in trees
20. Eggs hatch into froglets
F. Eggs in foam nest
21. Nest in burrow; subsequent to flooding, feeding tadpoles in ponds or streams
22. Nest in burrow; nonfeeding tadpoles complete development in nest
23. Nest arboreal; hatchling tadpoles drop into ponds or streams
G. Eggs carried by adult
24. Eggs carried on legs of male; feeding tadpoles in ponds
25. Eggs carried in dorsal pouch of female; feeding tadpoles in ponds
26. Eggs carried on dorsum or in dorsal pouch of female; nonfeeding tadpoles in bromeliads
27. Eggs carried on dorsum or in dorsal pouch of female; direct development into froglets
III. Eggs retained in oviducts
H. 28. Ovoviviparous
I. 29. Viviparous
*Egg deposifion site unknown; possibly have terrestrial eggs.

flood. Truly terrestrial foam nests in which nonfeeding that seen in the other families; the foam is kicked by the
tadpoles complete their development are characterisüc of hindlimbs of both males and females (Coe, 1974). The
Philoria frosti and the species of Kyarranus. In this aquatic viscosity of the nest and the hardening of the outer layer
to terrestrial sequence, there are a decrease in the num- of the foam in rhacophorids are more like the condi-
ber of eggs, an increase in the size of the ova, and a tion in leptodactylid nests than in the frothy nests of
decrease in the amount of pigmentaüon of the ova myobatrachids. The habit of constructing foam nests cer-
(A. Martin, 1967). tainly evolved independently in three groups of frogs and
The foam nests are constructed in different ways by presumably also independently in the Hyperoliidae, in
leptodactylids and myobatrachids (Tyler and M. Davies, which the only species known to construct a foam nest,
1979b); in the former the male kicks the foam with his Opisthoíhy/ox ¡mmacu/aíus, folds a leaf over the nest
feet, and in the latter the female creates currents and (Amiet, 1974).
foam with her hands. Some Oíd World tree frogs con- Direct development of terrestrial eggs may be preceded
struct arboreal foam nests, and at least the manner of evoluüonarily by nonfeeding tadpoles that complete their
construction in the rhacophorid Chiromantís differs from development in terrestrial nests. Direct development must
 Reproductive Strategies
37
Terrestrial
Ovoviviparity;
eggs; direct
viviparity development
(28)(29) (17)

Eggs and tads Foam nest on

Eggs and tads
carried by land;
terrestrial
adult terrestrial tads
(25)(26)(27) (15)06)
(22)

Foam nest on
Eggs terrestrial;
land; tads
tads aquatic
aquatic
(21)

Eggs and tads Eggs and tads

lotic lentic
(2) (1)

Eggs and tads Eggs carried by

carried by aquatic $
aquatic ?
(7)

Figure 2-5. Grades in the evolutlon of reproductive modes in anurans. Numbers in parentheses identify
modes defined in Table 2-2.

have evolved independently in at least 12 groups—min- Internal ferülization occurs in the species of Nectophry-
imally once each in the Leiopelmatidae, Pipidae, Soog- noides, but at least one species is oviparous with non-
lossidae, Myobatrachidae, Leptodactylidae, Bufonidae, feeding larvae, two are ovoviviparous, and two are vi-
Hylidae, and Rhacophoridae, and probably also in the viparous (Grandison, 1978; M. Wake, 1980a).
Brachycephalidae. Presumably, direct development There is a great diversity of reproductive modes in
evolved at least twice in the Ranidae (African arthrolep- some families (12 in leptodactylids, 11 in myobatrachids),
tines and Asiatic platymantines) and in the Microhylidae whereas nine families are characterized by a single mode
(Australo-Papuan asterophryines and genyophrynines, and (Table 2-3). It is evident that the trends away from the
Neotropical microhylines). generalized, primitive mode of eggs and tadpoles in ponds
Stages of specialization of different reproductive modes (Mode 1) does not necessarily represent increasing re-
are evident in certain groups. For example, within the productive specialization in phylogenetically advanced
egg-brooding hylid frogs there is a sequence of speciali- groups, but rather, many independently derived repro-
zation including hatching as feeding tadpoles, as non- ductive modes in different phyletic lines.
feeding tadpoles, or froglets (Duellman and Maness, 1980). The greatest diversity of reproductive modes is seen
LIFE HISTORY
among anurans in the tropics (Table 2-4). For example, different climatic regimes—from atmospherically drier to
in the United States only 4 modes are known, and 90% wetter environments {Duellman, 1982b) (Table 2-5).
of the species have eggs and tadpoles in ponds. How- Thus, in contrast to caecilians and salamanders, the
ever, at Santa Cecilia in Amazonian Ecuador 10 modes diversity of reproductive modes in anurans is more a
occur, and only 37% of the species have eggs and tad- reflection of the environmental regimes in which the frogs
poles in ponds (Salthe and Duellman, 1973). Within South live than of the phylogenetic relationships of the families
America, 21 reproductive modes are known, but 14 of and higher categories.
these are restricted to the tropical part of the conünent.
With the exception of Leiopelma in New Zealand and
Rhinoderma in southem South America, frogs at latitudes QUANTITATIVE ASPECTS
greater than 40° have aquaüc eggs and larvae. The great diversity in pattems and modes of reproduction
Ecologically, the generalized mode is most widespread in amphibians is associated with differences in fecundity,
in lowlands, whereas trends toward terrestrial modes be- duratíon of development, reproductive effort, and age at
come prevalent in highlands. Many terrestrial modes are first reproduction. In this interface between develop-
restricted to environments with continuously high atmos- mental and populaüon biology, amphibians are espe-
pheric moisture, as noted in the fidelity of so-called forest cially noteworthy because of their reproductive diversity
modes to rainforests and the lack of fidelity of nonforest and, in many species, complex life cycles.
modes (J. D. Lynch, 1979a). Within South America, the Adequate quantitaüve data on various parameters of
proporüon of different reproductive modes changes in amphibian life histories are available for only a few spe-

Table 2-3. Taxonomic Diversity of Reproductíve Modes in Anurans*

1 - + + + + + + - - + + - - + + - - + - + + 13
2 + - - - + - + - + + + --- + -- + + -- 9
3 _ _ _ _ _ _ i 1

4 - - - - - - -1-
T -U
~r 4-
~r ~ 9
O
5 _ _ _ _ _ _ _ _ _ _ l _ + _ _ _ _ _ _ _ _ _ _ _ 2
6 _ _ _ _ _ _ _l_ ^
7 _
8 _
_
_
_
_
_
_
_
_
_
_
+- i -_ _ __ +_ __ __ _ _ _ __ __ __ __ - _ | _ . __ __ 3i
9 _ _ _ _ _ _ + _ _ _ _ _ _ _ _ _ _ _ _ _ _ !
10 - - - + - - _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ i
11 - - - + - - 1

12 - - - - - - + _ _ _ _ _ _ _ _ _ _ + _ + _ 3
13 - - - - - - + __ + _ _ _ _ _ _ _ + _ + _ 4
1 4 _ _ _ _ _ _ _ _ _ _ + _ + _ _ _ + + _ _ _ 4
15 - - - - - - _ _ _ + + _ _ _ _ _ _ + _ _ + 4
16 - - - - - - + + _ _ _ _ + _ _ _ _ _ _ _ _ 3
17 + _ _ _ _ _ + + - + + ? - - - - - + + -+ 9
1198 _
- -
_ _- _- _- -
_ - - - - - - - - + + - + + + + 6
_ _ _ _ _ _ _ _ _ _ _ _ + + _ 2
20 - - - - - - _ _ _ + _ _ _ _ _ _ _ + _ _ _ 2
2i _ _ _ _ _ _ - ) - - - — - L _ _ _ _ _ _ _ _ _ _ _ _ ! _ _ _ Q

22 - - - - - - + __ + _ _ _ _ _ _ _ _ + + _ 4
23 - - - - - - - - + - - - - - - - - - + - - 1
24 _ + _ _ _ _ 1

25 - - - - - - _j_ 1

26 + 1
2 7_ _ _ _ _ _ _j_ 1

28 - - - - - - _ _ _ - ! - + _ _ _ _ _ _ _ _ _ _ £
2 9_ _ _ _ _ _ 1 ___ 1

Totals 2 8 1 1 9 8
*See Table 2-2 for defmitíons of modes.
 Reproductive Strategies
Table 2-4. Geographical Diveisity of Anuran Reproductiva Modes 29
Characteristic Nearctíc Palearctíc Neotropical Ethiopian Oriental Australo-Papuan
Number of modes 4 6 21 12 11 12
Percentage of modes 14 21 72 41 38 41
Unique modes 0 1 8 1 0 2
Percentage unique 0 17 38 8 0 17

Table 2-5. Modes of Reproduction of Anurans in Different Tropical Habitáis in South America

Seasonal Aseasonal Clond

Mode of reproduction Sav; rainforest* rainforest* foresf
Forest modes
Eggs and tadpoles in lotíc water6 10 (10.8%)
Eggs and tadpoles in tree cavltíes or bromeliads 1 (1.1%)
Eggs on vegetation above ponds; aquatic tadpoles' 1 (4:2%) 6 (19.4%) 15 (17.0%) 3 (3.5%)
Eggs on vegetation above streams; aquatic tadpoles 2 (2.3%) 11 (11.9%)
Eggs terrestrial; tadpoles to water on adults 3 (9.7%) 6 (6.9%) 9 (9.8%)
Eggs and tadpoles in terrestrial foam nest 1 (3.2%) 1 (1.1%)
Eggs terrestrial; direct development 1 (3.2%) 19 (21.7%) 49 (53.3%)
Eggs on dorsum of female; direct development 1 (1.1%) 8 (8.7%)

Nonforest modes
Eggs and tadpoles in lentic water 14 (58.3%) 16 (51.6%) 34 (38.6%) 1 (1.1%)
Eggs and early tadpoles in aquatic nest 1 (3.2%) 1 (1.1%)
Eggs in foam nest; tadpoles in ponds 9 (37.5%) 2 (6.5%) 7 (8.0%) 1 (1.1%)
Eggs on dorsum of aquatic female 1 (3.2%) 1 (1.1%)

Total—forest modes 1 (4.7%) 11 (35.5%) 45 (51.1%) 90 (97.8%)

Total—nonforest modes 23 (95.8%) 20 (64.5%) 43 (48.9%) 2 (2.2%)

Total—both modes 24 31 88 92
"El Manteco, Venezuela (Hoogmoed and Gorzula, 1979). dAmazonian slopes of Andes in Ecuador (Duellman, 1979) with additions.
6Belém, BrazU (Crump, 1971). ePerhaps some of these species deposit eggs on vegetation above streams.
cSanta Cecilia, Ecuador (Duellman, 1978) with additions. 'Some of these—species of Phyllomedusa—wrap leaves around their eggs.

cíes. These data are reviewed and discussed in the fol- more than 5,000 in A. tigrinum (F. Rose and Armentrout,
lowing paragraphs. 1976). At the other extreme, Salamandra aira usually
gives birth to only two young at a time (V. Vilter and A.
Fecundity Vilter, 1960). The variation in fecundity in frogs is also
It is well known that fecundity levéis are highly variable highly variable and is most closely associated with repro-
among amphibians. Generally, large species have more ductive mode, but also correlated with body size within
eggs than smaller ones. Also, species having generalized reproductive modes. Among species that have direct de-
reproductive modes produce larger clutches than those velopment of terrestrial eggs, the diminutive Sminthillus
that have specialized modes. This is exemplified in cae- limbatus of Cuba deposits a single egg per clutch (Noble,
cilians, in which the oviparous Ichthyophis glutinosas may 1931b), but other species having this mode deposit up
lay as many as 54 eggs in a single clutch (P. Sarasin and to 100 eggs or more. The ovoviviparous Eleutherodac-
F. Sarasin, 1887-90), but the viviparous Geotrypetes tylus¡aspen has only 3-5 eggs (M. Wake, 1978). Species
semphini may give birth to only one to four young (M. deposiüng eggs in water have much larger clutches, many
Wake, 1977a). Among salamanders, fecundity is highest thousands in some of the larger species of Bufo and Rana.
in species that deposit their eggs in water, much lower in The largest known clutches are produced by Rana ca-
those having terrestrial eggs, and lowest in those that give tesbeiana; one female having a snout-vent length of 179
birth to living young. For example, Siren lacertina may mm deposited a clutch of 47,840 eggs (McAuliffe, 1978).
deposit more than 500 eggs (Noble and Marshall, 1932), Size-fecundity relationships were described for sala-
and Cryptobranchus alleganiensis produces up to 450 manders by Salthe (1969) and for anurans by Salthe and
eggs in a clutch (B. Smith, 1907), whereas the largest Duellman (1973). Further observations and discussions
clutches in salamanders are produced by Ambystoma — were presented by Crump (1974), Kuramoto (1978a),
more than 1,000 in A. mexicanum (Gaseo, 1881) and Kaplan and Salthe (1979), and Kaplan (1980a). An ovar-
LIFE HISTORY
30 volume and volume of the mature ovarían complement,
0,
Oí O
regardless of reproductive mode (Rg. 2-6) (Crump, 1974).
E
Likewise, a significant positive correlation exists between
1 clutch size and female snout-vent length among species
c
2
•X*
m/
f
* of E/eutherodacty/us (M. Wake, 1978). Within species
/
<D 1

E '' there are similar significant correlations in some groups:

"o. Desmognathus (Tilley, 1968), Ambystoma (Kaplan and
E 0- ¿
Salthe, 1979), six species of pond-breeding frogs in
o /
o **p Michigan (Collins, 1975), and among various Japanese
c -i. O'
ro ' •o amphibians (Kuramoto, 1978a). On the other hand, sig-
(6 09 y'
nificant positive correlations exist in only 11 of 41 tropical
8 -2- 8ÍOD
/
species studied by Crump (1974), and no correlations
0}
O) y0' »Eggs aquatic exist in Hy/a rosenbergi (Kluge, 1981). This may be be-
5 -3- /° ° °Eggs not aquatic cause of the small ranges in sizes and/or ovarían com-
plements of many of the species, or possibly because of
- 1 0 1 2 3 4 5 6 variable amounts of energy available for reproduction.
There is a positive correlation between body size and
Loge Body Volume clutch size and ovarían complement in températe, ter-
restrial plethodontine salamanders and a similar trend in
Figure 2-6. Relationship between mean body volume of gravid tropical bolitoglossine salamanders (Fig. 2-7), but the
females and mean volume of mature ovarían complements in 23
species of anurans in Amazonian Ecuador. Y = 2.27 + 0.903 X; bolitoglossines have larger clutches than do plethodon-
r = 95.1 (P < 0.001). Modified from Crump (1974). tines of similar sizes (Houck, 1977b). The ova of the
tropical species generally are smaller than those of the
températe species.
Ovum-size-body-size relationships generally are not so
ian size factor (clutch size X ovum diameter/female snout- clear as the clutch- size relationships, except that as a
vent length) was proposed as an Índex of comparing general rule, at a given body size there is a negative
fecundity and egg size relative to adult body size (Duell- correlation between clutch size and ovum size. Nonethe-
man and Crump, 1974). less, some studies have shown significant interspecific and
The general conclusions concerning interspecific size- intraspecific correlations between ovum size and body
fecundity relationships are as follows: size—various anurans (Collins, 1975), Ambystoma
(Kaplan, 1980a), and E/euíherodacty/us (M. Wake, 1978).
1. Within a given reproducüve mode, there is a
positive correlaüon between clutch size and
female body size.
2. Within a given reproductivo mode, there is a
positive correlation between ovum size and 40-
female body size.
3. Regardless of reproductive mode, there is a
negative correlation between clutch size and Í30-
ovum size.
4. Regardless of reproductive mode, there is a
positive correlation between ovum size and o
c 20-
size of hatchlings. (O

§
O
Other correlations are considered in the following sec- 10-
tion: Duration of Development.
The most significant conclusión is the high correlation •-Tropical bolitoglossines
between body size and clutch volume. Weaknesses in o- o-Temperate plethodontines
the relationships between fecundity and body size, and
20 40 60 80 100 120
between ovum size and body size are the result of the
variable negative correlation between ovum size and Snout-Vent Length (mm)
fecundity. Figure 2-7. Size-fecundity relationships among plethodontid
Among anurans in the upper Amazon Basin in Ecua- salamanders having direct development of terrestrial eggs. Among
dor there is a significant positive correlation between body températe species, V = -8.60 + 0.368 X; r = 33.7 (0.025 < P <
0.05). Among tropical species, Y = -1.58 + 0.377 X, r = 62.4
length and fecundity in each of three reproductive modes, (P < 0.001). Difference in elevation of lines, t = 4.316 (P < 0.001).
and there is a significant positive correlation between body Based on Houck (1977b) with additions.
 Reproductiva Strategies
31
Eggs:
4- • Ponds
o Streams
A Arbórea I
• Terrestrial
I 3
o>

<D
o 24

Figure 2-8. Relationship of ovum

size and hatchling size in frogs. Each
symbol is the mean for a species.
6 8 10 12 14 16 Y = 1.18 + 3.18 X; r = 69.1 (P <
0.001). Modifled from Salthe and
Total Length at Hatching (mm) Duellman (1973).

5H ment. For example, in species of anurans having terres-

trial eggs undergoing direct development, the smaller eggs
hatch much more rapidly than larger ones (Fig. 2-9).
Among chorus frogs, Pseudacris triseriata, ovum size is
significantly larger and duration of development more
4- rapid in montane than in lowland populations (Pettus and
Angleton, 1967). Conversely, among four populations of
I three species of Ambystoma, egg size does not seem to
be correlated with rate of development to the feeding
§
¿o stage at various controlled temperatures, but larger larvae
3-
develop from larger ova and absolute differences in size
become amplified with time (Kaplan, 1980a).
Basing their generalizations on frogs that deposit eggs
in water and on K. Bachmann's (1969) investigations,
2- Salthe and Duellman (1973) concluded that there is a
negative correlation between ovum size and rate of de-
velopment This is an oversimplification. The eggs of most
frogs develop much faster than do those of salamanders.
The developmental time to hatching in aquatic eggs of
15 25 35 45
salamanders ranges from about 15 days in some Am-
Duration of Development (Days) bystoma to 275 days in Dicampíodon ensatus; terrestrial
Figure 2-9. Duration of development in eggs of 12 species of eggs undergoing direct development require from 60 days
anurans having direct development. Y = 9.85 + 7.03 X; r = 32.1 in some small species of Plethodon to 250 days in Bo/i-
(P < 0.05).
toglossa compacta (Table 2-6). On the other hand, among
anurans, aquatic eggs require from only 1 day in various
Data on ovum size and size of hatchling are limited but Bu/o, Hyla, and Scaphiopus to 42 days in Rana aurora,
show a positive correlatíon among species of frogs having whereas terrestrial eggs undergoing direct development
different reproductive modes (Fig. 2-8). Also, intraspecific require from 15 days in Eleutherodactylus to 49 days in
and intrapopulatíonal correlaüons have been demon- P/otymantis hazelae (Table 2-7). Notable exceptions among
strated in various species of Ambystoma (DuShane and frogs are the high Andean marsupial frog, Gostrotheca
C. Hutchinson, 1944; Kaplan, 1979, 1980a), Tritunts riobambae, in which the eggs require about 88 days to
vulgaris (G. Bell, 1977), and Rhyacotriton o/ympicus develop into tadpoles, and the egg-brooding Pipa pipa,
(Nussbaum and Tait, 1977). in which 107 days on the average are required for the
eggs to develop into froglets.
Duration of Development Rate of development and therefore duration of devel-

I Within reproductive modes there are some apparent cor-

relatíons between ovum size and duraüon of develop-
opment are temperature-dependent. Aside from the work
of K. Bachmann (1969), various studies have demon-
LIFE HISTORY
strated thc negative correlaüon between developmental that of eggs developing in water.
rate and temperatura. For example, Ambystoma opacum Conflicting results were obtained by Moore (1939),
requires about 250 hours at 20°C from gastrula to halch- who demonstrated that cold-adapted species of North
ing, but at 10°C this development requires about 800 American Rano and Ambysíoma have faster rates of de-
hours (Kaplan, 1980a). Spadefoot toads have extremely velopment than warm-adapted species. These results are
rapid development; at 30°C, the eggs of Scaphiopus cou- supported by data on alütudinal variatíon in development
chii and S. bombifrons hatch in 15 and 20 hours, re- of A, macrodactylum (J. Anderson, 1967) and R. tem-
spectively, but at 10°C, 82 and 84 hours, respecüvely, poraria (Kozlowska, 1971). Experimenta by Berven et al.
are required for development to hatching (Justus et al., (1979) on development of eggs of R. clamitans from
1977). different elevations demonstrated that eggs from high
In the small marsupial frog, F/ecíonoíus pygmaeus, the elevations develop faster at low temperatures than do
eggs are about 4.4 mm in diameter and require 24 or eggs from low elevations; however, in natural situations,
25 days to develop to hatching at Stage 41 (staging ac- eggs develop more slowly at high elevations because the
cording to Gosner, 1960), whereas in Gastrotheca riob- water temperature is lower. Thus, the relaüonships that
ambae, eggs are about 3.0 mm in diameter and require exist between ovum size and duration of development
88 days to hatch at Stage 25 (Duellman and Maness, are affected by temperature and some other factors, which
1980; del Pino and Escobar, 1981). These differences at the present time are unknown. Perhaps in the large
are not entirely temperature-dependent. The average terrestrial eggs that hatch into advanced young, part of
temperature in the cloud forest where F/ecíonoíus lives the relatively immense caloric contení of the egg helps
is higher than that at Quito, Ecuador, where G. riob- lo speed development
ambae was studied. However, eggs of F/ecíonoíus de-
veloped in 29 days at Quito. Obviously, in these frogs Reproductive Effort
and others having large eggs that contain sufficient yolk The measure of effort in terms of parenlal invesrmenl of
for development to a froglet, some mechanism or prop- time in courtship and mating, proportional weighl ( =
erty of the egg (possibly rales of protein synthesis or energy) devoled lo eggs, and amounl of caloric inlake
enzyme activily) increases the rate of development over required for gametogenesis and vitellogenesis are all as-

Table 2-6. Fecundity and Development in Selected Salamanders (Mean Valúes)

Duration of
development Percent snrvival
Clatch Egg
laays; of young of
Species size (mm) Egg Larva adnlt témale Soorce
Eggs and larvae aquatíc
Hynobius nebulosas" 128 2.00 27 138 31.2 Thom (1963)
Cryptobranchus alleganiensis° 450 6.00 76 1750 22.7 Bishop (1941)
Siren intermedie? 200 3.00 270 24.4 Noble and Marshall (1932)
Notophthalmus viridescens 302 1.50 —
28 84 63.1 Bishop (1941)
Trituras uulgaris 241 1.50 20 86 56.7 G. Bell and Lawton (1975)
Necturus macu/osus 107 5.50 57 1750 67.8 Bishop (1941)
Ambystoma macrodactylum 307 — 25 115 J. Anderson (1967)
Ambystoma maculatum 134 2.75 43 87 —
27.8 Bishop (1941)
Dicamptodon ensatus 138 6.00 275 700 41.0 Nussbaum (1969a)
Rhyacotríton o/ymp/cus 8 3.20 250 990 80.0 Nussbaum and Tait (1977)
Leurognathus mamoratus 38 3.00 83 450 58.0 Martof (1962b)
Eurycea multiplícate 13 2.50 32 195 90.0 P. Ireland (1976)

Eggs terrestrial; larvae

aquatic
Ambystoma opacum 150 2.70 41 255 Bishop (1941)
Desmpgnathus ochrophaeus 16 3.00 71 150 25.0 Organ (1961); Tilley (1972)
Hemidacfylium scutatum 50 2.75 56 42 30.0 Bishop (1941)

Eggs terrestrial; direct

development
Aneides aeneus 17 4.50 87 — R. Cordón (1952)
Bolitoglossa rostrata 37 3.50 165 — —
34.3 Houck (1977a)
Boütoglossa subpalmata 23 5.00 135 — 17.3 Vial (1968)
Desmognathus aeneusb 11 1.90 40 15 23.9 J. Harrison (1967)
Ensatina eschscholtzi 13 3.90 120 — 29.0 Stebbins (1954) .
Plethodon cinereus 9 3.00 56 — 29.3 Sayler (1966)
Plethodon glutinosus 21 4.25 60 — 20.7 Highton (1962)
Tertilization extemal. 'Nonfeeding terrestrial larvae.
 Reproductiva Strategies
pects of reproductíve effort, as is the investment in pa- mature later than males; most of the exceptions are spe- 33
rental care, if any. Theoretically, species of the same size, cies in which both sexes mature early. The greatest age
having the same reproducüve mode, and living in the (5 years) at which males become reproductive are in the
same climatic regime should devote approximately the paedomorphic, aquatic cryptobranchids and proteiids;
same amount of energy to reproduction. Variables, such females require 6 years, but some males and females of
as the size and number of eggs and number of clutches, Triturus uulgaris do not reproduce until their seventh year
then would be a reflectíon of age (= size) and relative (G. Bell, 1977). The earliest-maturing salamander is the
health of the female. Any deviations from this pattern aquatic plethodontid Eurycea multiplicata, both sexes of
would indícate a change in reproductive effort, and changes which are sexually mature shortly after metamorphosis
in reproductive mode (e.g., small aquatic eggs to large at an age of 5-8 months (P. Ireland, 1976). As a group,
terrestrial eggs) or reproductive pattems (e.g., semelpar- the porid-breeding Ambystoma mature relatively early
ity to iteroparity) would suggest modiftcaüons in repro- (1-3 years), and salamandrids mature much later (3-6
ductive effort. years). Within the plethodontids, those species having
Empirical evidence on the energeücs of reproduction aquatic larvae generally mature earlier (0.5-4 years for
in amphibians is extremely limited. In Desmognathus males and 0.5-5 years for females) than do those having
ochrophaeus an esümated 68.5% of the annual second- direct development of terrestrial eggs (1.75-6 years for
ary production in mature females is devoted to produc- males and 1.75—12 years for females).
üon of eggs (Fitzpatrick, 1973a). Caloñe content of eggs Among anurans, the greatest ages at attainment of sex-
of different species of Ambystoma vanes independently ual maturity are in species at high latitudes or altitudes;
of clutch volume (Kaplan, 1980b). Comparaüve studies males may require 4 years and females as many as
on the energy content of eggs of Neotropical Hyla (Crump 6 years. On the other hand, species in aseasonal, humid
and Kaplan, 1979) revealed that the energy contained in tropical lowlands mature much earlier. The earliest nor-
each clutch (relative to female body size) is not signifi- mal maturation reported is 6-7 months in males and
cantly different ii. species depositing eggs in ponds from 9 months in females of Rana erythraea (W. Brown and
those placing their eggs on vegetation over ponds; small Alcalá, 1970). Quite probably, many small hylids and
species expend proportionately the same amount of en- hyperoliids mature even faster. Precocious reproduction
ergy as larger species. However, there is a noticeable may occur at an age earlier than normal, such as at 80-100
difference in the partitioning of energy within the clutches. days postmetamorphosis in Limnodynastes íosmaniensis
Those species that deposit clutches in ponds have about (Horton, 1982a). Age at first reproduction in 12 tropical
twice the number of eggs per clutch as those that place species of anurans is 6-15 months (mean = 10.79) in
their clutches on vegetation. The arboreal eggs contain males and 8-15 months (mean = 10.99) in females,
* about twice the caloric content of the aquatic eggs and whereas in 25 midlatitude températe species the valúes
require longer to hatch into larger, more advanced tad- are 1-2.5 years (mean = 1.54) in males and 1-3 years
poles. (mean = 1.83) in females. By contrast, the ages of 8
species at high latitudes and high elevations in the tem-
Age and Reproduction pérate regions are 2-4 years (mean = 3.44) in males
The age that an individual enters the reproductive pop- and 2.5-6 years (mean = 3.69) in females.
ulatíon and the span of its reproductive life are importan! Differences in climatic regimes are reflected in age at
factors in a reproductive strategy. Although the existing sexual maturity in some species having broad geographic
data are limited, some patterns are evident in salaman- or altitudinal ranges. Latitudinal gradients show a delay
ders and anurans. Because so little information is avail- in maturation of 2 years in Bu/o calamita from Switzer-
able, it is not possible to discem patterns within the cae- land to Sweden and in Rana pipiens from southern to
cilians. Females of Geotrypetes seraphini and Dermophis northern Michigan. Likewise, lowland populations of
mexicanos apparentiy breed for the first time at 2 years Ambystoma macrodacty/um and Desmognathus ochro-
of age, whereas males of the latter species presumably phaeus mature a year earlier than their respective high-
do not breed until they are 3 years oíd (M. Wake, 1977a, land populations. A 2- to 4-year difference in age at first
1980b). Earlier maturation by females compared with reproduction occurs between lowland and highland pop-
males is contrary to data for any salamanders and anu- ulations of Rana sylvatica in Maryland.
rans. Females of Dermophis have a long gestation period Some of the species that require the longest time to
and certainly do not reproduce every year, whereas males mature have lengthy larval periods. Thus, among sala-
have continuous gametogenesis. Because never more than manders, Rhyacotriton o/ympicus breeds at an age of
half of the females are reproductively active, early matu- 4.5-5 years, but 3-3.5 of those years are spent as a larva
ration of females is advantageous in maintaining a higher in cold streams. Likewise, Ascaphus truel spends 3 years
proportion of reproductive females in the population. as a tadpole in cold streams before metamorphosing to
Most salamanders do not reproduce before the age of reproduce in its fourth year. The age at first reproduction
2 years, whereas many frogs reproduce at the age of 1 in fíana catesbeiana depends on the length of the larval
year (Tables 2-8 and 2-9). In most species the females period—one or two overwinterings; young frogs usually
Table 2-7. Fecundity and Development in Selected Anurans (Mean Valúes)
Dnration of development (days) Percent survival
Clntch Egg Nonfeeding Feeding of yonng
Species Size (mm) Egg larva larva adult témale Source
Eggs and larvae aqnatic
Ascaphus trueP 37 4.00 30.0 — 1080 47.0 Noble and Putnam (1931)
Bambino bambino 100 2.00 12.0 — 90 36.5 Berger and Michalowski (1963)
Hymenochirus boettgeri 450 0.75 2.0 — 42 — G. Rabb and M. Rabb (1963)
Pelobates fuscus 750 1.50 5.5 — 120 48.3 Berger and Michalowski (1963)
Macrogenioglottis alipioi 3650 1.50 2.5 — 107 Abravaya and Jackson (1978)
136 3.5 — —
— Wager (1965); J. Visser (1971)
Heleophryne purceltf 3.50 730
Bufo canorus 1750 2.00 5.5 — 50 17.6 Karlstrom (1962)
Bufo quercicus 500 1.09 1.0 — 26 — Volpe and Dobie (1959)
Bufo valliceps 4100 1.23 3.8 — 24 10.2 Limbaugh and Volpe (1957)
Nectophrynoides osgoodi 307 2.75 10.0 — 27 — Grandison (1978)
Hyla auiuoca 650 1.17 1.7 — 24 25.0 Volpe et al. (1961)
Hy/a cinérea 700 1.20 2.0 — 35 44.0 Garton and Brandon (1975)
Hyla crucifer 900 1.10 6.0 — 45 32.2 Gosner and Rossman (1960)
Hyla rosenbergib 2350 1.95 2.8 — 33 24.6 Kluge (1981)
Limnaoedus ocularis 100 0.95 3.5 — 42 48.8 Gosner and Rossman (1960)
Litaría verreawá 731 1.23 6.1 — 90 36.2 Anstís (1976)
Phrynohyas venulosa 2920 1.60 1.0 — 42 23.6 Pyburn (1967)
Pseudacris brachyphona 646 1.60 4.6 — 55 25.0 N. Creen (1938)
Pseudacris streckeri 601 1.40 4.5 — 60 32.5 Bragg (1942)
Smilisca cyanosticta 1167 1.20 1.0 — 40 22.6 Pyburn (1966)
Phrynobatrachus natalensis 650 1.00 3.5 — 28 Wager (1965)
2.0 — 49 — Wager (1965)
Ptychadena oxyrhyncha 350 1.30 —
Pyxicepha/us adspersus 3500 2.00 2.0 — 18 20.0 Wager (1965)
Rana areolata 6000 1.84 10.8 — 150 31.3 Volpe (1957c)
Rana aurora 838 3.04 42.0 — 100 26.8 Storm (1960)
Rana cancrivora 2527 1.25 3.4 — 63 20.0 Alcalá (1962)
Rana euerettP 925 2.15 6.6 — 105 25.3 Alcalá (1962)
Rana fuscigula 15,000 1.50 8.5 — 1080 — Wagner (1965)
Rana japónica 1700 1.75 21.0 — 90 Okada (1966)
14.0 — 85 — F. Tumer (1958)
Rana pretíosa 539 2.40 —
Rana septentrionalis 509 2.30 4.0 — 360 42.8 Hedeen (1972)
Rana sylvatica 1750 1.90 20.0 — 67 30.8 Stebbins (1951)
Tomoptema delalandii 2500 1.50 3.0 — 35 19.4 Wager (1965)
Hyperolius marmoratus 350 1.30 5.0 — 49 — Wager (1965)
Kassina macúlala 300 1.50 6.0 — 270 80.0 Wager (1965)
Kassina senegalensis 400 1.20 5.5 - — 90 62.0 Wager (1965)
Anodonthyla bou/engerf 27 2.00 8.0 18.0 44.7 Blommers-Schlosser (1975b)
800 1.6 — —85 24.2 Alcalá (1962)
Ka/ouía con/uncía 1.10
Phrynomerus bi/asciaíus 600 1.30 4.0 — 30 Wager (1965)
— — Blommers-Schlosser (1975b)
Platypefís grandis0 100 4.00 19.0 16.0 14.4
P/ethodontohy/a notostictrf7 120 3.00 14.0 14.0 — 15.0 Blommers-Schlosser (1975b)

Egg* in foam not; larvae

aqnatic or in neat
Kyarranus sphagnico/a 48 3.25 10.0 20.0 Moore (1961)
Limnodynastes peroni 857 1.45 6.0 — 150 Moore (1961)
Megisto/otis /ignarius" 352 1.87 2.5 — 122 43.1 Tyler et al. (1979)
Phi/oria /rostí 95 3.90 9.0 40.0 14.2 Littlejohn (1963)
Physa/aemus cuuleri 419 1.90 3.0 — 60 Boktmunn (1962)
Chiromanfls petera?1 325 1.00 4.0 — 157 Coe (1974)
Polypedates /eucomystaxd 175 1.85 3.3 1.0 90 —
29.7 Alcalá (1962)
Rhacophorus pordalis0 46 3.00 7.7 1.7 83 28.1 Alcalá (1962)

Eggs terrestrial or arboreal;

larvae aquatic
Alytes obstetricansf 63 3.10 30.0 — 360 13.7 Crespo (1979)
Nectophryne afra 26 3.50 7.0 — 28 — Scheel (1970)
Nectophrynoides malcolmi 18 2.60 18.0 17.0 — — Grandison (1978)
Colostethus trínítatus1 12 3.50 21.0 — 56 Kenny (1969a)
Dendrobates /emora/is' 23 2.00 14.5 — 48 —
— Polder (1976)
Dendrobates silverstonei^ 30 2.00 11.2 — 74 Myers and Daly (1979)
14 11.0 — 55 —
30.1 Myers et al. (1978)
Phyllobates terribilis' 2.50
Phyllobates vittatus1 14 2.50 15.0 — 25 — Silverstone (1976)
Agalychnis callidryas 51 2.25 5.0 — 74 32.0 Pyburn (1963)
Hyla bertha/utzae 52 3.00 5.0 — 50, 37.5 Bokermann (1963)
Phyllomedusa trinitatus 536 3.25 7.4 — 77 28.1 Kenny (1966, 1968)
Arthroteptella hewitti 30 3.00 17.0 3.0 10.5 Wager (1965)
—
Rana magna0 178 2.60 6.3 — 83 17.9 Alcalá (1962)
Rana microdisccf 47 2.00 7.5 — 55 32.7 Alcalá (1962)
Mantidacty/us líber 60 1.40 6.0 — 60 41.8 Blommers-Schlósser (1975a)
Afrixalus fomasinii 80 2.00 5.0 — 90 50.0 Wager (1965)
Hyperolius pusillus 310 1.00 5.0 — 42 Wager (1965)
60 — Wager (1965)
Hyperolius tuberitinguis 400 1.50 5.0 — —
Eggs terrestrial;
development dlrect
Leíopelma archeyí 9 4.50 44.0 — — 35.5 N. Stephenson (1951b); D. Bell
(1978)
Eleutherodactylus martiae 9 3.30 26.0 — — 22.7 Crump (1974)
Eleutherodactylus planirostris 17 2.00 15.6 — — 24.0 C. Goin (1947)
Eleutherodactylus 7 3.50 30.0 — — 25.6 Crump (1974)
pseudoacuminatus
Hylactophryne augusti 67 4.20 35.0 — Jameson (1950)
—
— —
18.2 Wager (1965)
Anhydrophryne rattray't 15 2.60 28.0 —
Arthroleptís wahlbergi 21 2.50 28.0 — — 25.0 Wager (1965)
Platymantis guentherí 8 3.00 39.0 — — 16.4 Alcalá (1962)
Platymantis hazelae 7 3.40 49.0 — — 33.9 Alcalá (1962)
Platymantis meyerí 27 3.30 39.0 — — 17.3 Alcalá (1962)
Breviceps adspersus 33 4.50 35.0 — — 15.0 Wager (1965)
Myersiella microps 12 3.00 29.0 — — — Izecksohn et al. (1971)

Eggs carricd by témale

Pipa pipa9 83 6.00 107.0 — — — G. Rabb and Snedigar (1960)
Flectonotus pygmaeus 9 4.40 24.5 13.0 — 27.7 Duellman and Maness (1980)
Gastrotheca riobambae 128 3.00 88.0 — 360 37.0 del Pino and Escobar (1981)

Eggs retained in oviducts

Eleutherodactylus jasperí 4 3.30 33.0 — — 36.3 Drewry and K. Jones (1976)
Nectophrynoides occidentalis1* 8 0.60 270.0 — — 31.0 Lamotte et al. (1964)
Tadpoles in streams. "Eggs carried on legs of male.
bEggs and early larval stages in nest. 'Tadpoles carried by adult from terrestrial nest to water.
cEggs and larvae in water in tree boles or leaf axils. 9Aquatic.
dFoam nest arboreal. hViviparous.
LIFE HISTORY
36 Table 2-8. Age at First Reproduction in Selected Salamanders
Age in years
from hatching
Species Hales Females Source

Ranodon sibiricus 4 4 Bannikov (1949)

Salmandrella keyserlingi 3 4 Steward (1970)
Ananas japónicas 4 5 Tago (1929)
Cryptobranchus alleganiensis 5 6 Bishop (1941)
Siren intermedia 2 2 W. Davis and Knapp (1953)
Notophthalmus viridescens 2 2 " Healy (1974)
(without eft)
Notophthalmus viridescens 4-8 4-8 Healy (1974)
(with eft)
Pleurodetes walti 2 3 Steward (1970)
Salamandra otra 3 4 Thorn (1968)
Salamandra salamandra 3 4 Thorn (1968)
Taricha torosa 3 3 McCurdy (1931)
Tríturus cristatus 3 3 Steward (1970)
Trituras vulgaris 3-7 3-7 G. Bell (1977)
Necturus maculosus 5 6 Bishop (1941)
Ambystoma macrodactylum 2 2 J. Anderson (1967)
(coastal)
Ambystoma macrodactylum 3 3 J. Anderson (1967)
(highland)
Ambystoma maculatum 1 2 Husting (1965)
Ambystoma opacum 1.3 1.3 Bishop (1941)
Ambystoma tigrinum 1 1 Bishop (1941)
Rhyacotriton olympicus* 4.5-5 4.5-5 Nussbaum and Tait (1977)
Amphiuma tridactylum 4 Cagle (1948)
— 4
Desmognathus fuscus 3 Danstedt (1975)
Desmognathus ochrophaeus 3 4 Tilley (1973)
(lowland)
Desmognathus ochrophaeus 4 5 Tilley (1973)
(highland)
Desmognafhus 3.5 5 Organ (1961)
quadramacu/atus
Desmognathus twrighti 3.5 5 Organ (1961)
Leurognathus marmoratus 2 3 Martof (1962b)
Eurycea íongicauda 1.5 3 J. Anderson and Martíno
(1966)
Eurycea multiplicata 0.5-0.7 0.5-0.7 P. Ireland (1976)
Eurycea neotenes 2 2 Bruce (1976)
Eurycea quadridigitata 0.5 0.5 J. Harrison (1973)
Hemidactylium scutatum 2.3 2.3 Blanchard and Blanchard
(1931)
Pseudotríton montanus 1 4^5 Bruce (1975)
Pseudotriton ruber 4 5 Bruce (1978b)
Stereochilus marginatus 3 4 Bruce (1971)
Aneides flavipunctatus 3.3 4.3 Houck (1977b)
Batrachoseps attenuatus 2.5-3 3.5 Maiorana (1976a)
Bolitoglossa rostrata 2.5 3.7 Houck (1977a)
Bolitoglossa subpalmata 6 12 Vial (1968)
Ensatina eschscholtzi 3 3.5 Stebbins (1954)
Plethodon cinereus 1.7 1.7 Sayler (1966)
Plethodon glutinosas (Honda) 2.5 3 Highton (1962)
Plethodon glutinosus 4.5 5 Highton (1962)
(Maryland)
Plethodon hoffmani 2.3 3.3 Angle (1969)
Plethodon vehiculum 2.7 3.3 Peacock and Nussbaum (1973)
Plethodon wehrlei 4 4-5 Hall and Stafford (1972)
*3-3.5 years as larva.

reach sexual maturity within a year after metamorphosis. reach sexual maturity in 2.5 years, but if the subadult
Many températe frogs breed for the first time in the sea- loses its tail, where fat is stored, or faces an adverse year,
son following hatching, so many are less than 1 year oíd age at first reproduction may be delayed 1 year (Maior-
at the time of their first reproduction. ana, 1976a).
The fossorial salamander Batrachoseps attenuatus may Early versus delayed maturation can depend on certain
 Reproductíve Strategies
TaMe 2-9. Age at First Reproducüon in Selected Anurans 37
Age from hatching
Species Males Females Source
Ascaphus truel" 4yr 4yr Metter (1964a)
Bambino bombina 2yr 2yr Bannikov (1950)
Discoglossus pictus 2yr 3 yr Knoeppfler (1962)
Hymenochirus boettgeri 12-18 mo 12-18 mo G. Rabb and M. Rabb (1963a)
Pipa carvalhoi 7-9 mo 7-9 mo Weygoldt (1976a)
Scophiopus holbrooki 1-2 yr 1-2 yr P. Pearson (1955)
HeKoporus eyrei 2yr 2yr A. Lee (1967)
Megisto/otis lignarias 10 mo 10 mo Tyler et al. (1979)
Ekutherodactylus johnstonei < 1 yr < 1 yr Chibon (1962)
Ekutherodactyíus planirostris < 1 yr < 1 yr Goin (1947)
Leptodactylus macrostemum 1 yr 1 yr Dixon and Staton (1976)
Bufo americanas 2-3 yr 3yr Hamilton (1934)
Bu/o calamita (Sweden) 4yr 4 yr Gislén and Kauri (1959)
Bu/o calamita (Switzerland) 2yr 2yr Heusser and Meisterhans (1969)
Bu/o canorus 3yr 3yr Karlstrom (1962)
Bu/o maririus 1 yr lyr G. Zug and P. Zug (1979)
Bu/o quera'cus lyr 2yr Hamilton (1955)
Bu/o valliceps < 1 yr < 1 yr W. Blair (1953)
Bufo woodhousü 2yr 3yr Underhill (1960)
Phylhbates terribilis 13 mo 13 mo Myers et al. (1978)
Acris crepitans < 1 yr < 1 yr Collins (1975)
Hyh chrysoscelis 1-2 yr 2yr S. Roble (pers. comm.)
Hyla cinérea < 1 yr < 1 yr Cartón and Brandon (1975)
Hyla crucifer lyr 1 yr Collins (1975)
Hyla regula lyr — Jameson (1956)
Hyla rosenbergi < 1 yr < 1 yr Kluge (1981)
Hyla versicolor 2yr 2yr Collins (1975)
Pseudacris triseriata < 1 yr < 1 yr S. Roble (pers. comm.)
Gastrophryne carolinensis 1 yr 1-2 yr P. K. Anderson (1954)
Gastrophryne olivácea 1-2 yr 1-2 yr Fitch (1956)
Ptychadena maccarthyensis 8-9 mo 8-9 mo Barbault and Trefaut R. (1978)
Ptychadena oxyrhyncha 8-9 mo 8-9 mo Barbault and Trefaut R. (1978)
Rana aurora 2yr 2yr Storm (1960)
Rana catesbeianab 2-3 yr 3 yr Collins (1975)
Rana clamitans 1-2 yr 2yr Martof (1956)
Rana erythraea 6-7 mo 9 mo W. Brown and Alcalá (1970)
Rana pipiens (N. Michigan) 4yr 4 yr Forcé (1933)
Rana pipiens (New York) 2yr 2yr R. Ryan (1953)
Rana pipiens (S. Michigan) 1-2 yr 1-2 yr Collins (1975)
Rana preíiosa 4yr 5—6 yr F. Tumer (1960)
Rana septentriona/is 2yr 2-^3 yr Hedeen (1972)
Rana sylvatica (low Maryland) 1 yr 2yr Berven (1981)
Rana sylvatica (S. Michigan) 1-2 yr 2yr Collins (1975)
Rana sylvatica (high Maryland) 3-4 yr 3-4 yr Berven (1981)
Rana temporaria 3yr 3yr Heusser (1970b)
°3 years as larva. *1 or 2 years as larva.

aspects of the life history. A classic example is the newt breed at the age of 1 year but produce fewer and smaller
Notophthalmus viridescens, in which most populations eggs than older females (Kawamura et al., 1972). Fe-
have a terrestrial, subadult, eft stage lasting 2-6 years, males of Discog/ossus pictus first breed at 3 years of age,
after which the salamanders become aquatic and breed when they produce one or two clutches of no more than
for the flrst time at an age of 4—8 years. Some coastal 300 eggs each; older females produce up to six clutches,
populations omit the terrestrial eft stage and reach sexual, each with as many as 800 eggs, per season (Knoeppfler,
maturity at the age of 2 years (Healy, 1974). 1962). Clutches of 12-year-old Tríturus vulgaris contain
Older females contribute more offspring than younger four times as many eggs as those produced by 3-year-
ones, not only because they are larger and have larger olds; furthermore, older females produce larger eggs
clutches, but because they may contribute more clutches (G. Bell, 1977).
in a breeding season. Females of Rana catesbeiana in Next to nothing is known about the reproductive life
their flrst breeding season produce only one clutch, spans of amphibians. The most notable exception is Hyla
whereas many older females produce two clutches rosenbergi in Panamá, which reproduces in the rainy sea-
(R. W. Howard, 1978b). Females of Bombina orienta/is son following hatching at the age of less than 1 year
LIFE HISTORY
38 (Kluge, 1981). At that time témales may lay up to six span is about 16 years, so the máximum offspring ex-
clutches of eggs in about 150 days; essenüally no females pected in this species is only eight.
survive for a second breeding season. The average clutch Very little is known about the proportion of females in
size is 2,350, so a female may produce about 14,100 a population that breed in any given season. Theoreti-
eggs during her reproductive life span. Female Rana ca- cally, in those salamanders having biennial reproductive
tesbeiana in southern Michigan have an adult life ex- cycles, about half of the females breed in any given year.
pectancy of 4 years; they deposit one clutch the first year If age at first reproduction is relatively constant within a
and potentíally two clutches in succeeding years (Collins, population, then all females in a given cohort would be
1975; R. W. Howard, 1978b). The mean clutch size is expected to breed in the same year. With few exceptions,
11,636 eggs (Collins, 1975), so one female might pro- female anurans breed every season, and the indication
duce more than 80,000 eggs in her life. Rana sylvatica from limited data on species inhabiting aseasonal, humid
in Maryland exhibits an entirely different pattern; most tropical regions is that individuáis breed frequently, as
females breed only once, after 2 to 4 years of growth, often as every 2 or 3 weeks in some species.
and deposit a single clutch of about 2,500 eggs (Berven,
1981).
Generally, salamanders live longer than frogs; a Cryp- PARENTAL CARE
íobranchus a//egan¡ens¡s was reported to have survived By comparison with birds and mammals, amphibians
for 55 years in capüvity (Nigrelli, 1954). Females of this generally have been thought to exhibit little parental care.
species reproduce for the first time at an age of 6 years, However, in recent years both field and laboratory stud-
and they have annual clutches of about 450 eggs (Bishop, ies have provided evidence for an astonishing array of
1941). By combining the longevity record and the clutch parental care in amphibians. Parental care may be de-
size, we can arrive at a potential life-time fecundity of fined as any behavior exhibited by a parent toward its
22,500 eggs—a highly unlikely occurrence in nature. Fe- offspring that increases the offspring's chances of survival
male Ambystoma macu/atum may breed for 5 consecu- (Trivers, 1972); this investment may reduce the parent's
tive years in southern Michigan (Husting, 1965); clutches ability to invest in additional offspring. Among amphibi-
contain about 200 eggs, giving this species a potential ans, parental care includes attendance of the eggs, trans-
producüon of about 1,000 offspring during its life. A portation of eggs or larvae, and feeding of larvae. Paren-
plethodontid, such as Ensatína eschscho/te¡, which lives tal care is associated only with those species that place
to at least 7 years but requires 3 years to reach sexual their eggs in single clusters, never with those that scatter
maturity, will produce three clutches of about 13 eggs their eggs in aquatic situations. Nest construction, either
each biennially, for a total of about 39 eggs during its prior to or during oviposition, is not considered to be
life. Salamandra atra requires 4 years to reach sexual parental care, although in some species that construct
maturity and then produces two living young at intervals nests, one parent may attend the eggs. Likewise, the
of usually 4 years (V. Vilter and A. Vilter, 1960). The life retention of eggs in the oviducts, even though nourish-

Table 2-10. Diversity of Parental Care ¡n Amphibians

Parental care of Investing parent
Eggs Larvae Site of care Caedlians Salamanders Anurans Remarks
+ - Aquatic — 4 ó", 12 9 33 —
+ — Aquatic foam nest — — 13 —
+ + Aquatic foam nest — — 19 9 with school of larvae
+ - Aquatic nest 33 $ constructs and guards nest
+ - Terrestrial 5—9 3—9 4<í Larvae aquatic
+ - Arboreal — — ±11 ó", 9 Larvae aquatic
+ + Terrestrial — 19 6Í, 9 Nonfeeding larvae
+ + Arboreal — — 63 Nonfeeding larvae
+ - Arboreal foam nest 19 Larvae aquatic
+ - Terrestrial 4—9 — 9
± 175 ±50 3, 9 Development direct
+ - Aquatic — — 5? Eggs on dorsum
+ + Aquatic — — 29 Eggs and larvae in stomach
+ - Terrestrial
— — 2 ó" Carried on hindlimbs
+ - Terrestrial/arboreal — — 55 $ On dorsum or in dorsal pouch
- + Terrestrial
— — ±75 3, 9 Transported to water on dorsum
— + Terrestrial — — 39 Transported to water on dorsum
and subsequently fed
- + Terrestrial
— — 1 <J Transported to water in vocal sac
— + Terrestrial — — 13 Develop in vocal sac
- + Terrestrial
— — 1 ó* Develop in inguinal pouches
- + Terrestrial — — 19 Develop on dorsum
 Reproductiva Strategies
39

Figure 2-10. Female caecilian,

Ichthyophís glutinosas, coiled about
eggs ¡n burrow. From F. Sarasin and
P. Sarasin (1887-90).

ment is provided to the developing young, is not consid- aeraüon of aquaüc eggs, manipulaüon and/or moistening
erad to be parental care. of terrestrial eggs, protection against predators, and re-
In amphibians, parental care is widespread phyloge- moval of dead or infected eggs. Among the few species
netically and is especially diverse in anurans (Table exhibiting parental care of aquatic eggs, males of Cryp-
2-10). Parental care has been reported in only about tobranchus and Hynobius are territorial and drive away
10% of the species of frogs and in only a few caecilians all conspecifics except gravid females (Kerbert, 1904;
(Rg. 2-10), but it occurs in the majority of salamanders. B. Smith, 1907; Thom, 1962). Captíve male Ananas
Most commonly, parental care is associated with those japónicas have been observed to agítate the eggs
fcogs that have prolonged breeding periods and with frogs (Stejneger, 1907). Either sex of the subterranean Proteus
and salamanders characterized by terrestrial modes of anguineus may attend the eggs; these aquatic salaman-
reproduction. In caecilians and salamanders, parental care ders wave their tails so as to direct water currents over
consists solely of attendance of cggs, usually by the fe- the eggs (Vandell and Bouillon, 1959; Durand and Van-
male. This same behavior occurs in anurans; however, dell, 1968). In aquaria, Necturus maculosus jostle their
compared with salamanders and caecilians, a greater eggs by periodically waving their gills near the eggs (Salthe
number of frog species have males in the attendance of and Mecham, 1974); females of this species also protect
egg clutches. Attendance of eggs may be facultaüve— their eggs from conspecific oophagy (Bishop, 1926).
ihe eggs are capable of developing without the attendant Similar agitation of aquatic eggs by water currents gen-
parent, but survivorship may be enhanced by the pres- erated by kicking the feet is known in the toad Necfo-
ence of the parent. Only in anurans does parental care phryne afra (Scheel, 1970). Agitation of aquatic eggs has
involve the transportation of eggs and larvae. Most, if not been interpreted as aeration, but oscillation of the eggs
aü, of the parental care involving transportation of eggs may be necessary for normal embryonic development,
and larvae is obligatory. Complex behavior of oviposiüon as shown for terrestrial salamander eggs (Forester, 1979).
and/or morphological and physiological modiflcaüons are Males of the African "hairy" frog, Tríchobatrachus ro-
associated with such parental care. bustus, have been observed sitting on egg clutches in
Parental care in amphibians was reviewed by Salthe streams (Perret, 1966).
and Mecham (1974); this behavior in frogs was discussed Female attendance at egg clutches in streams is known
by Lamotte and Lescure (1977), McDiarmid (1978), and for the salamander Dicamptodon ensatus (Nussbaum,
Wells (1981a), and in salamanders by M. Ryan (1977) 1969a) (Fig. 2-11) and several plethodonüd salamanders:
and Forester (1979). species of Gyrinop/ii/us (Bruce, 1978a), Pseudotriton
(Bruce, 1978b), Eurycea (Franz, 1964), Leurognathus
Diversity of Parental Care (Martof, 1962b), and Desmognathus (Oigan, 1961).
Parental attendance at egg clutches has various roles in However, parental attendance of aquatic eggs is un-
different species or at different sites. Functions include known in Ambystoma and salamandrids.
LIFE HISTORY
40

Figure 2-11. Femóle salamander,

Dicamptodon ensatas, attending eggs
under log in stream. Photo by E. D.
Brodie, Jr.

Figure 2-12. Nest oíHyla boans

shnwing surface film of eggs; the
nest is scooped out by a male, which
subsequently defends the nest agalnst
intruders. Photo by W. E. Duellraan.

Male attendance at aquatic foam nests by the myo- in Leptodactylus ocellatus is a precursor to protection
batrachid frog Adelotus brevis may be simply a conse- afforded to the tadpoles. In this species the tadpoles move
quence of territoriality, but males have long tusks on the about in dense masses; the female remains with the tad-
lower jaw that might be used in effective protection of poles and attacks wading birds attempting to feed on the
the eggs. Likewise, the presence of the male myoba- tadpoles (Vaz-Ferreira and Gehrau, 1975). The large,
trachid Pseudophryne bibronii in burrows containing eggs aggressive African ranid Pyxicepha/us adspersus has been
seems to be a territorial funcüon; any protection resulting reported to protect tadpoles in shallow ponds by driving
in greater survivorship of the eggs is secondary (Wood- away potential predators (B. Balinsky and J. Balinsky,
ruff, 1977). Female attendance at an aquatic foam nest 1954). However, this apparently is only aggressive be-
 Reproductive Strategies
41

Figure 2-13. A centrolenid,

Centrolcnella sp., attending an egg
clutch on the underside of a leaf over
a stream. Photo by W. E. Duellman.

havior, because Pyxicepha/us will eat the tadpoles (Amiet, 1981), but by males in the leptodactylid Thoropa
(Wager, 1965). petropo/iíana (Heyer and Crombie, 1979), the bufonid
The best-documented study of male attendance of Nectophrynoides ma/co/mi (Grandison, 1978), in three
aquatic eggs is that of the nest-building gladiator frog, species of the ranid genus Petropedetes (Amiet, 1981),
Hyla rosenbergi (Kluge, 1981). Males are highly territorial and in the microhylids P/ethodontodohy/a tuberaía
and aggressive, and they cali from shallow basins that (Blommers-Schlósser, 1975b), Breviceps adspersus
they scoop out of soil adjacent to water. Eggs are de- (Wager, 1965), and Synapfuranus sa/seri (Pybum, 1975).
posited as a surface film on water in the basin (Fig. 2- The eggs of three Madagascaran microhylids P/aíype/is
12). If the surface tensión is broken, the eggs sink to the grandis, P/ethodoníohy/a notosticta, and Anodonthy/a
bottom of the basin and die of oxygen deprivation. Males boulengeri, which develop and hatch in water in tree
patrol the nest áreas and attack intruding conspecific males, holes or leaf axils, are all attended by males (Blommers-
whose entry into the nest can disrupt the surface tensión. Schlósser, 1975b). Female Leptodactylus fallax remain
The facultativo nature of this parental care is demon- with eggs and larvae in a terrestrial foam nest (G. Brooks,
strated by significantly higher rates of guarding in a year 1968; Lescure, 1979). Larvae that are essentially im-
of high populaüon density than in a succeeding year of mobile on a disintegrated terrestrial nest or confined to
low density. a constrained aquatic situation (e.g., leaf axil or tree hole)
In Amphiuma the habit of coiling about the eggs and are susceptible to many predators; thus, guarding the
holding them free of the substrate at times of drying of offspring may be the primary purpose of the attending
the nest is thought to aid in preventing desiccation of parent. The provisión of moisture to the eggs and larvae
eggs (J. Weber, 1944). The terrestrial eggs of Dendro- also may be a function in those species having terrestrial
bates auratus and D. pumi/io are periodically moistened nests. However, parental care has not been observed in
by males emptying their bladders on the clutch (Wells, the myobatrachid genus Kyarranus, which has terrestrial
1978a; Weygoldt, 1980). Presumably the ranid Hemisus nests and nonfeeding larvae, in leptodactylids of the ge-
marmoratum also provides moisture for developing eggs; nus Adenomera having direct development in terrestrial
the female sits on the clutch in a subterranean chamber foam nests, or in egg-brooding hylids that place non-
and, subsequent to the hatching of the tadpoles, digs a feeding tadpoles in leaf axils.
tunnel to water, thereby allowing the tadpoles to escape Centrolenid frogs of the genus Centrolenella breed on
from the nest chamber (Wager, 1965). vegetation overhanging streams; in many species the males
Attendance of developing eggs and nonfeeding larvae are territorial, and in some they attend the eggs (Fig. 2-
in terrestrial nests is a behavior common to several kinds 13). Centrolenella co/ymbiphy//um and C. valeríoi are
of frogs and one salamander, Desmognathus aeneus. Care sympatric in Costa Rica; males of the former attend egg
is exhibited by the female in Desmognathus (J. Harrison, clutches on the undersides of leaves only at night, whereas
1967), in the leptodactylid Zachaenus paruus (Heyer and males of the latter remain with the eggs night and day
Crombie, 1979), and in the ranid Phrynodon sandersoni (McDiarmid, 1978). The eggs are preyed upon by a small
LIFE HISTORY
42

Figure 2-14. West Indian

leptodactylid, male Eleutherodactylus
hedricki, attending a terrestrial
clutch. Photo by M. M. Stewart.

wasp, which presumably is deterred by the presence of

a male. In 112 clutches of C. valerioi, only 7% of the
eggs were lost, compared with 23% among 152 clutches
of C. co/ymbiphy//um. Pernales of Hyperolius obstetrí-
cans remain with their eggs on leaves overhanging streams;
upon hatching, the female kicks the tadpoles out of the
jelly (Amiet, 1974). Pernales of the West African ranid
Phrynodon sandersoni attend eggs on leaves of bushes
at night (Amiet, 1981). In the rhacophorid Chiromantis
xerampe/ina, a female has been observed periodically
moistening the arboreal foam nest (W. Rose, 1962).
The eggs of Ambystoma opacum develop in a terres-
trial depression with an attending female, who occasion-
ally agítales the eggs and moves about on the eggs; the
área of movement is free of fungus (Salthe and Mecham,
1974). The eggs are abandoned when the nest floods
and the larvae hatch. Pernales of the plethodontid sala-
manders Hemidactyhum scutatum and Stereochilus mar-
ginatus attend egg clutches in sphagnum moss or rotting i?-,, •
logs above water; upon hatching the larvae escape into Figure 2-15. Female plethodontid salamander, Pseudoeurycea
the ponds (Blanchard, 1934; G. Rabb, 1956). juarezi, attending an egg clutch originally beneath stone. Adapted
Parental attendance of terrestrial eggs that undergo di- from a photo by R. W. McDiarmid.
rect development is widespread among anurans and nearly
universal in terrestrial plethodontid salamanders. Male at- males attend the eggs (Jameson, 1950), whereas in Geo-
tendance occurs in some species of Eleutherodactylus, at bafrachus walkerí females are the attendants (Ardila-
least some of which (e.g., E. caqui and £. hedricki) are Robayo, 1979). Males of Leiopelma archeyi and perhaps
territorial and rnay attend more than one clutch at a time also L. hochstetteri sit on clutches (E. Stephenson and
(Drewry, 1970; Townsend et al., 1984). In many others, N. Stephenson, 1957), whereas in sooglossid frogs and
females sit on, or adjacent to, eggs in leaf litter or under in the bufonid Oreophrynella females attend the clutches
rocks (Fig. 2-14), or, as in £. caryophyí/aceus, perch on (Nussbaum, 1983; McDiarmid, pers. comm.). Among the
top of eggs adhering to a leaf on a bush (Myers, 1969). Australo-Papuan microhylid frogs, all of which have di-
In other leptodactylids, such as Hy/actophryne augusti, rect development of terrestrial or arboreal eggs, only males
 Reproductiva Strategies
attend the eggs in two species of Phrynomantis, two of tend terrestrial eggs that hatch into aquatic larvae (Sar- 43
Cophixalus, and three of Sphenophryne (Méhely, 1901; asin and Sarasin, 1887-90); the eggs sometimes are in-
Tyler, 1963a; Zweifel, 1972a; M. P. Simón, pers. comnn.), fected with fungi, and attendant females will eat eggs
but both parents attend the eggs in two species of Or- (Breckenridge and Jayasinghe, 1979). Female ¡diocran-
eophryne and one of Cophixalus (van Kampen, 1923; ium russeli coil about their eggs on small mounds in a
Zweifel, 1956; Simón, 1983). Only females of C. riparius dense mat of grass (Sanderson, 1932); these eggs undergo
attend eggs (M. P. Simón, pers. comm.). In the South direct development. Possibly, recently bom young of some
American Myersiella microps, only the female remains viviparous caecilians may be attended by the female;
with the terrestrial eggs (Izecksohn et al., 1971). Sanderson (1932:222) reported finding a female
Among the terrestrial plethodonüd salamanders, egg Geotrypes seraphini sitting on a mound in a chamber
clutches are usually attended by females (Salthe and Me- partially filled with water and wrapped around "a bundle
cham, 1974). Male attendance of some clutches and fe- of smaller replicas of herself, all with their heads pointing
male attendance of others occurs in Bo/itog/ossa subpal- toward her tail."
mata (Vial, 1968). In all closely observed cases, the Among amphibians, all known cases of mobile paren-
attending adult is in physical contact with the eggs, usu- tal care involve transportation of eggs and/or larvae by
ally with the chin in contact with the clutch and the body male or female frogs. With the exception of the aquatic
wrapped around it (Fig. 2-15); periodically, the adult ro- pipids, all such parental care is associated with terrestrial
tates the eggs in the clutch (Stebbins, 1954; Highton and eggs. In Pipa (Fig. 2-16) the eggs are carried on the
T. Savage, 1961; Vial, 1968; Tilley, 1972; Forester, 1979). dorsum of the female (G. Rabb and Snedigar, 1960;
This parental care has been thought to contribute to the Weygoldt, 1976a). Australian myobatrachids of the ge-
survival of the young by (1) protecüng them from pre- nus Rheobatrachus are unique in that the eggs and larvae
datíon, (2) preventing or reducing their infecüon by phy- develop in the stomach of the female (Corben et al.,
comycete fungí, or (3) agitating them to enhance aeration 1974; MacDonald and Tyler, 1984), and the young froglets
and/or prevent adhesive malformation. Conspecific oop- emerge from the mouth (Tyler and Cárter, 1981). In
hagy is common among plethodontid salamanders, and addition to the unique trait of gastric brooding, these are
eggs also are eaten by other species of salamanders and the only frogs known to carry both eggs and tadpoles.
various kinds of arthropods. Aggressive defense of clutches Egg-carrying by terrestrial male frogs is known only for
against predators has been observed in Aneides, Pleth- the European A/yíes. At the time of oviposition, the strings
odon, and Desmognathus (R. Cordón, 1952; Highton of eggs adhere to the hindlimbs of the male (Fig. 2-17).
and T. Savage, 1961; F. Rose, 1966). Numerous authors
have noted that terrestrial eggs of plethodontid salaman-
ders and anurans develop fungal infections in the ab-
sence of a parent, but anüfungal properties have not been
discovered in skin secretíons (Vial and Prieb, 1966, 1967).
The contributions of parental care in Desmognathus
ochrophaeus have been tested rigorously in field and
laboratory experiments by Forester (1979). Results of
these studies demónstrate conclusively that female at-
tendance contributed significantly to survivorship of the
clutches. Unattended clutches disappeared within a few
days, but when attendants and clutches were protected
from predators by confinement, survivorship increased
Figure 2-16. Female Pipa carvalhoi with eggs imbedded in
by 40% over unconfined controls. Dead eggs became dorsum.
infected by fungus, which subsequently attacked other
eggs in unattended clutches. Attendant females ate dead
and infected eggs, thereby restraining the spread of fun-
gus to other eggs. Furthermore, eggs in advanced stages
of development had a higher resistance to fungal infec-
tions; possibly, as first suggested by Highton and T. Sav-
age (1961), the embryos produce an anüfungal sub-
stance. It was also notíced that an attendant female places
her chin on the egg clutch, thereby subjecting the eggs
to slight vibrations caused by pulsations of the throat.
Clutches that were vibrated experimentally in the ab-
sence of females exhibited survivorship higher than that
of controls. Figure 2-17. Male Alytes obstetricians with eggs adherent to
Among caecilians, female ¡chthyophis glutinosus at- hindlimbs.
LIFE HISTORY
44

Figure 2-18. Egg-carrying in hylid frogs. A. In

dorsal pouch of female of Gastrutheca cornuta.
B. On dorsum of female of Hemiphractus
johnsoni.

He carnes the eggs and periodically enters the water;

when the larvae begín to hatch, the males sits in water
and the hatchlings are released (Boulenger, 1897; Crespo,
1979). All other egg-carrying is obligatory in females of
hemiphractíne hylids; in some of tríese the developing
eggs are in a dorsal pouch, and in others they are ad-
herent to the dorsum (Fig. 2-18). In the arboreal species,
development is direct in Gastrotheca and Amphignath-
odon, but terminales in nonfeeding tadpoles that are de-
posited in water in leaf axils in F/ectonotus and Frite/ana
In terrestrial species of Hemiphractus, Cryptobatrachus,
Stefania, and some Gastrotheca, development is direct.
In other high montane, terrestrial Gastrotheca, the eggs
hatch into tadpoles; at the time of hatching the females Figure 2-19. Male Colostethus subpunctatus carrying tadpoles;
move to ponds and reléase the tadpoles (Duellman and note that the ventral surfaces of the tadpoles are adherent to the
Maness, 1980). Buccal brooding of eggs in Leptope/is parent.
breuirostris was reported by Boulenger (1906), who found
eggs equal to the size of those in the oviducts in the involved in attachment (Stebbins and Hendrickson, 1959).
mouth of a female, but Noble (1926) noted that this In the myobatrachid Assa dar/ingíoni, nonfeeding tad-
specimen had been eviscerated through the mouth and poles wriggle up the legs and into inguinal pouches in
that remnants of the ovary and ovarían eggs were present the male, which carnes them unül they complete their
in the mouth. development (G. Ingram et al., 1975). Males of the two
External tadpole-carrying apparently is universal in the species of Rhinoderma transport tadpoles in their vocal
Dendrobatidae and otherwise is known in only six spe- sacs. In both species the hatching tadpoles are picked out
cies. Tadpoles adhere to the dorsum of either sex in den- of the deteriorating jelly of the terrestrial egg clutch. In
drobatids, males of Rana microdisca finchi (Inger, 1966), R. darwinii, nonfeeding tadpoles complete their devel-
and females of the leptodactylid Cyc/orhamprius stejne- opment in the vocal sac and emerge as froglets, whereas
geri (Heyer and Crombie, 1979) and Soog/ossus sey- males of R. ru/um simply transport tadpoles from the nest
chellensis (Nussbaum, pers. comm.). In the last species, to water (Formas et al., 1975).
the tadpoles complete their development on the dorsum, Parental care is complex in dendrobaüd frogs, all of
whereas in all of the others the parents reléase the tad- which are diurnal and transport tadpoles; furthermore,
poles in water. In all instances in which tadpoles have one or both sexes of many species are territorial and
been observed attaching themselves to the dorsum of the aggressive. Male attendance at clutches occurs in Colos-
parent, the adult sits in the remainder of the gelatinous tethus, such as C. subpunctatus (Stebbins and Hendrick-
egg clutch, and the tadpoles wriggle up the hindlimbs son, 1959). Males of Dendrobates auratus, D. pumilio,
and onto the back. The venter of the tadpole is adherent and Phyllobates vittatus, and females of D. histrioni'cus,
to the dorsum by a sticky mucus; the larval mouth is not lehmanni, and pumilio periodically wet their terrestrial
 Reproductive Strategies
clutches by emptying the contente of their bladders on ing them away, as in the case of oophagous salamanders, 45
the eggs (Wells, 1978a; Weygoldt, 1980; H. Zimmer- or by eating various invertebrates that might devour the
mann and E. Zimmermann, 1981). Upon hatching, the eggs. In these cases the parent actually is guarding the
entire complement of tadpoles is carried by males of Co- eggs. In terrestrial nests, attendant párente also may eat
lostethus collaris, nubicola, palmatus, subpunctatus (Fig. dead eggs that are infected with fungus, thereby reducing
2-19), trinitatus, Phyllobates terribilis, and P. vittatus the chance of fungal infecüon of other eggs in the clutch.
(Stebbins and Hendrickson, 1959; Durantand Dole, 1975; Protection from desiccation is afforded terrestrial eggs by
Luddecke, 1976; Myersatat, 1978; Wells, 1980b, 1981a; the attendant parent actively moistening the eggs, as in
H. Zimmermann and E. Zimmermann, 1981). Similarly, Dendrobates, or passively by placing its body between
entire complemente are carried by females of C. inquin- the eggs and the dry substrate (Amphiuma means) or dry
a/is and C. pratti (Wells, 1981a). In all of these species air (Eleutherodactylus). Osmotic transfer of water from
of Colostethus and Phyllobates the tadpoles are trans- parental üssue across egg capsules in E. coqui is regulated
ported to streams or, in the case of C. subpunctatus, by differences in osmotic pressures of the parent and the
small ponds. The tadpoles of Dendrobates develop in eggs (Taigen, 1981). The term "brooding" might best
water-filled leaf axils of various kinds of plante, including be reserved for those frogs that carry eggs or tadpoles
terrestrial and arboreal bromeliads, tree holes, or other and provide gaseous exchange between parental and
constrained containers. Many tadpoles are transported at embryonic tissues. This applies to the egg-brooding hy-
a time by males of Dendrobates auratus, azureus, fe- lids (del Pino et al., 1975) and pipids (Weygoldt, 1976b)
moralis, and pawulus (Polder, 1974; Wells, 1978a; and presumably to Assa, Rheobatrachus, and Rhino-
Duellman, 1978). Paternal versus maternal transporta- derma.
üon of tadpoles may be related to interspecific differences In frogs, parental care usually is associated with small
in territoriality (Wells, 1981a), and in some Dendrobates clutches, but there are some excepüons. The gladiator
it possibly is associated with subsequent maternal care. frogs of the Hyla boans group, males of which construct
Females of Dendrobates pumilio, histrionicus, and leh- and defend nests, have clutch sizes within the range of
manni carry individual tadpoles to sepárate water-filled variation of other Hyla of their size that do not exhibit
leaf axils of bromeliads; no tadpole is placed in an axil parental care. Also, egg and tadpole attendance by fe-
already containing a tadpole. Once all of the tadpoles males of Leptodacty/us ocellatus is not correlated with a
have been dispersed, the mother periodically oviposits reduction in clutch size.
unfertilized eggs in the water of the leaf axils containing The duraüon of care for a given clutch of eggs is highly
her tadpoles; she can maintain as many as six tadpoles variable (Table 2-11). Salamanders generally have a much
through metamorphosis, requiring 6 to 8 weeks of feed- longer period of care than do frogs—possibly up to
ing a complement of eggs at least twice to each tadpole. 8 months in Bolitoghssa compacta and to 9 months in
The presence of an adult on the leaf of the bromeliad Dicamptodon ensatus in cold mountain streams. Dura-
and subsequently entering the water in the leaf axil elicits üon of care in frogs usually is no more than 1 month,
a caudal vibraüon from the tadpole; this vibratíon pre- but there are two notable exceptions. Pipa pipa may carry
sumably signáis the tadpole's presence to the female eggs for more than 4 months, but these develop directly
(Graeff and Schulte, 1980; Weygoldt, 1980; H. Zim- into frogs. Gostroíheca ríobambae lives in cool Andean
mermann and E. Zimmermann, 1981). habitats and carries eggs in the pouch for up to 4 months
Dendrobates are the only amphibians known to feed before they hatch into tadpoles; development and brood-
their young, but bromeliad-dwelling tadpoles of the Cen- ing can be reduced by half at warmer temperatures in
tral American Hyla zeteki (E. Dunn, 1937) andAnofheca the laboratory (Duellman and Maness, 1980).
spinosa (E. Taylor, 1954) eat frog eggs, presumably those The habit of gastric brooding in Rheobatrachus silus
of their own species (Duellman, 1970), as do four Ja- and uitellinus elimínales the possibility of feeding during
maican hylids with bromeliad-dwelling tadpoles (E. Dunn, brooding; the entire digestive system shuts down. Female
1926a) and the African microhylid Hoplophryne rogersi salamanders attending clutches may feed on small or-
with eggs and tadpoles in cavities in bamboo or in leaf ganisms near the oeste and on infected eggs; they also
axils (Noble, 1929a). Possibly maternal provisión of un- make short forays away from the nest, but brooding
ferülized eggs for nutrition of tadpoles occurs in these plethodontids in eastern North America are deprived of
species and also in a Philautus (Wassersug et al., 1981). food in relatíon to conspecifics (Organ, 1961a; Krzysik,
The oophagous tadpoles of these taxa have relatively 1980). Dendrobatíds actively feed while attending clutches
large beaks and reduced denudes (absent in Hoplophryne). and carrying tadpoles, and Alytes and egg-brooding hy-
lids feed while carrying eggs. Little information is avail-
Interpretation of Parental Care able on the energetic coste of egg attendance. There is a
The most common form of parental care among am- reduction in lipid contení in fat bodies in Desmognathus
phibians is the attendance of the egg clutch by one par- ochrophaeus during 6 weeks of attendance of clulches
ent. In some cases, it is known that the parent physically (Filzpalrick, 1976), Ihereby indicaling Ihal even if Ihe
protects the eggs from potential predators, either by driv- salamanders are feeding, their caloric intake is not suffi-
LIFE HISTORY
46 dent to maintain their normal metabolism. On the other production in females of other species of frogs exhibiting
hand, no significant caloñe loss is evident in females of maternal care is unknown. However, paternal care of
Ambystoma opacum attending eggs (Kaplan and Crump, eggs or tadpoles commonly is associated with more than
1978); howcver, at the time of attending eggs, no adults one clutch in a season or even more than one clutch at
of this species are feeding. a time. Even in the cool forests of New Zealand, Leio-
The cost of investment in one clutch of eggs or group pelma archeyi normally has two clutches each season
of larvae may have effects on frequency of reproduction. that are attended by males (E. Stephenson and N. Ste-
Annual or biennial reproductive cycles in salamanders phenson, 1957). Adults of Alytes obstetricans breed two
are associated with long periods of maternal care. Like- to four times each summer; the interval between breed-
wise, females of Gastrotheca and Pipa pipa have an an- ings is peaked at about 1 month—the duration of egg-
nual reproductive cycle (G. Rabb and Snedigar, 1960; carrying by the males (Crespo, 1979). Males of Dendro-
del Pino, 1980b). but pipids that produce tadpoles re- bates, Eleutherodactylus, and Centrolenella are known
produce several times a year (Sughrue, 1969; Weygoldt, to attend more than one clutch simultaneously (Drewry,
1976a). Females of Colostethus inguinalis produce two 1970; Wells, 1978a; McDiarmid, 1978). Males of Hyla
clutches per year (Wells, 1980a). The frequency of re- rosenbergi defend nests for only two or three nights, dur-

Table 2-11. Duration of Parental Care in Selected Salamanders and Anurans

Taxon Sex Days Kind of care Source

Salamanders
Cryptobranchus alleganiensisf 3 68-84 Aquatíc nest Bishop (1941)
Necturus maculosusf 1 38-57 Aquatic nest Bishop (1941)
Dicamptodon ensatus" 9 275 Aquatic nest Nussbaum (1969)
Leurognathus marmoratus" 9 75-90 Aquatic nest Martof (1962)
Eurycea bis/meato" 9 67-70 Aquatic nest Bishop (1941)
Ambystoma opacum" 9 41-52 Terrestrial nest Bishop (1941)
Hemidacfyl'mm scutatum" 9 52-60 Terrestrial nest Bishop (1941)
Desmognat/ius ochrophaeus" 9 52-69 Terrestrial nest Tilley (1972)
Desmognathus aeneus 9 ±50 Terrestrial nest J. Harrison (1967)
Bo/itog/ossa compacta 9 250b Terrestrial nest Hanken (1979)
Bo/itog/ossa rostrata 9 150-180 Terrestrial nest Houck (1977a)
Bo/itog/ossa subpa/mafa 9 120-150 Terrestrial nest Vial (1968)
Ensatina eschscholtzü 9 ± 120 Terrestrial nest Stebbins (1954)
Plethodon cinereus 9 60-65 Terrestrial nest Highton and T. Savage (1961)
Plethodon vehiculum 9 ±60 Terrestrial nest Peacock and Nussbaum (1973)

Anurans
Adelotus brevisf c? 6 Aquatic foam nest J. Moore (1961)
Nectophryne afra0 d 35 Aquatic nest Scheel (1970)
Hyla rosenbergi" e? 2-3 Aquatic nest Kluge (1981)
Hemisus marmoratum" 9 10 Terrestrial burrow Wager (1965)
Breuiceps adspersus" 9 28-42 Terrestrial burrow Wager (1965)
Leiope/ma archeyi <J 42 Terrestrial nest E. Stephenson and N. Stephenson (1957)
Eleutherodactylus caqui ¿ 17-26 Terrestrial nest Townsend et al. (1984)
Hylactophryne angustí ¿ 25-35 Terrestrial nest Jameson (1950)
Thoropa petropolitana" ó" 10-12 Terrestrial nest Heyer and Crombie (1979)
Nectophrynoides malcolmi $ 35 Terrestrial nest Grandison (1978)
Cophíxalus parkerí á, 5 85-100 Terrestrial nest Simón (1983)
Myersiella microps 9 29 Terrestrial nest Izecksohn et al. (1971)
Dendrobatos auratus" (J 10-13 Terrestrial nest Wells (1978a)
Dendrobates puntillo" ó" 10-12 Terrestrial nest Weygoldt (1980)
9 42-56 Ovipositing for tadpoles Weygoldt (1980)
Platypelis grandis" d 35 Eggs and tadpoles in tree hole Blommers-Schlósser (1975b)
Plethodontohyla notosticta" á 28 Eggs and tadpoles ¡n tree hole Blommers-Schlosser (1975b)
Anodonthyla boulengerf <j 26 Eggs and tadpoles in tree hole Blommers-Schlósser (1975b)
Alytes obstetricans" á 30 Eggs on hindlimbs Crespo (1979)
Pipa carua/hoi° 9 14-28 Eggs on dorsum Weygoldt (1976a)
Pipa parua" 9 30 Eggs on dorsum Sughrue (1969)
Pipa pipa 9 77-136 Eggs on dorsum G. Rabb and Snedigar (1960)
F/ectonotus pygmaeus" 9 24-25 Eggs in pouch Duellman and Maness (1980)
Gastrotheca riobambae" 9 103-120 Eggs in pouch del Pino et al. (1975)
Rheobaírachus si/us 9 37 + Eggs and tadpoles in stomach Corben et al. (1974)
Assa dar/ingtoni ó" 7+ Tadpoles in pouch G. Ingram et al. (1975)
Colostethus ¡nguina/is" 9 8-9 Tadpoles on dorsum Wells (1980a)
"Aquatic larvae. bLaboratory; female not in attendance.
 Reproductiva Strategies
ing which time they do not breed; this interval of not is associated with external fertilization, especially when 47
advertising may reduce a male's chances for a successive fertilization and oviposition occur in the male's territory.
matíng (Kluge, 1981). This hypothesis is generally and broadly applicable to
Communal nests, composed of eggs deposited by sev- amphibians. The numerous apparent exceptions may be
eral females, are known in the bufonid Nectophrynoides owing to our limited knowledge of parental care and ter-
malcolrm attended by a male and in the plethodontids ritorial behavior, especially among anurans.
Batrachoseps attenuatus and Hemidactylium scutatum A high degree of paternal investment in care of eggs
attended by females. There is no evidence that the at- or young may lead to a reversal of the usual sex roles.
tending male Nectophrynoides is the parent of all clutches The behavior in Dendrobates auratus is consistent with
that he attends (Grandison, 1978). Aggregations of fe- the idea of sex-role reversal; males are not territorial,
males of the microhylid frog Sphenophryne mehelyi at- attend eggs, and transport larvae, and females compete
tend their individual clutches of eggs (Tyler, 1967). The for males and produce small clutches at frequent intervals
factors contributing to egg attendance at communal nests (Wells, 1978a, 1981a). Other anurans may exhibit sex
are not known. R. Harris and Gilí (1980) suggested that role reversal, but there is no evidence for it. Attendance
successively intruding females of Hemidactylium could of eggs and transportation of larvae are restricted to males
drive away and eat some existing eggs prior to ovipos- in Assa darlingtoni and in the two species of Rhinoderma,
iting, but the selective advantages of such a behavior but the roles of females in these species are not known.
seem to be obscure. The communal sites for terrestrial
species such as Sphenophryne mehe/yi may provide bet-
ter physical conditions than surrounding áreas. Rana syl- EVOLUTION OF
vatica deposits eggs in ponds, but does not attend the REPRODUCTIVE STRATEGIES
clutches. Most clutches are deposited communally; eggs Theories on the evolution of life-history phenomena and
transplanted into a pond before oviposition had begun reproductive strategies have been expanded over the years
there resulted in all subsequent egg deposiüon at the site to encompass not only fecundity but trophic level, de-
of the introduced eggs (R. W. Howard, 1980). mography, survivorship, and environmental predictability
Among frogs, paternal care is most noticeable in ter- (see L. Colé, 1954; Stearns, 1976; and Wilbur et al.,
ritorial species: dendrobaüds, some Eleutherodactylus, 1974, for reviews). Wilbur (1977a:43) summarized the
some Centrolenella, and gladiator frogs (Hyla boans ideas, as follows: "A 'reproductive strategy' is a set of
group). A male that defends a restricted territory can pro- 'tactics' that has been selected as the adaptations that
vide care for egg clutches with little additional investment. have contributed, on the average, the greatest number
In dendrobatid frogs, different parental care is affected of offspring to recent generations. Each strategy involves
by males and females with respect to territorial behavior compromises in the allocation of resources between cur-
by the sexes. As emphasized by Wells (1981a), a frog rent reproduction and the potential for future reproduc-
transporüng tadpoles is unlikely to defend a territory. Thus, tion. The benefit of current reproduction is balanced by
in those species in which the male is highly territorial and its cost to adult growth, future fecundity, and adult sur-
may attend the eggs, it is the female that transports the vival. The cost may involve the direct mortality risks of
tadpoles to water. In other species, females are territorial, current reproduction or the long-term reduction in adult
and the male transports the tadpoles. Males of Assa and longevity incurred by shifting resources from mainte-
Rhinoderma brood tadpoles, but it is unknown if they nance and growth to current breeding demands."
are territorial. Egg-brooding by hylids, pipids, and Rheo- As emphasized by Crump (1982), a major factor in
batrachus is accomplished by females and apparently is reproductive strategies is the predictability of the envi-
unrelated to territoriality. With the exception of Necto- ronment relative to each stage of the life history. Organ-
phrynoides malcolrm and Eleutherodactylus caqui, in which isms with complex life cycles demónstrate contrasting
fertilization is intemal and males attend clutches, all known reproductive responses in stable versus fluctuating envi-
cases of parental care in anurans are associated with ex- ronments, depending upon which stage is affected by the
temal fertilization; either sex may provide care. The only environmental instability. Thus, from theory on repro-
known instances of paternal care in salamanders are spe- ductive strategies, the general predictions are that in sta-
cies that have external fertilization. Only maternal care is ble environments (1) late maturity, (2) múltiple clutches,
known in caecilians and in salamanders with intemal fer- (3) fewer but larger eggs, (4) parental care, and (5) small
tilization; in these groups, oviposition may occur several reproductive efforts should be favored, whereas in fluc-
months after mating. tuating environments the opposite correlates should ob-
Various hypotheses have been proposed to explain the tain. The former is the classical K-selection and the latter
evolution of maternal versus paternal care (see Gross and is r-selection in the sense of MacArthur and E. Wilson
Shine, 1981, and Wells, 1981a, for reviews). G. Williams (1967) and Pianka (1970). However, life history patterns
(1975) proposed that associatíon with the developing may vary depending upon age-specific mortality. If the
embryos preadapts a sex for parental care. Thus, in those environment of juvenile stages is unstable, resulting in
groups having internal fertilization, it is usually the female high and/or unpredictable mortality, different strategies
that is associated with the young; paternal care most often will be favored than in environments that are uncertain
LIFE HISTORY
for adults, resulting in high and/or unpredictable mortality Early age at first reproduction usually is an indication
at that stage (see B. Low, 1976, for application to am- of fluctuating or low juvenile survivorship, uncertain
phibians). High reproducttve success in one season may breeding conditions, and/or fluctuating population den-
result in greater density of adults in the following, or sub- sities. Notable differences in life-history patterns obtain in
sequent, season, in which case male-male interacüons lowland versus highland populations of Rana pretiosa
may be intensified and resources for successful repro- (L Licht, 1975). In the lowlands, where the entire repro-
ductíon may be limited. ductive effort may be lost in any given year because of
Differences in patterns of egg deposition, fecundity, drought, the females mature in 1-2 years and breed an-
and parental investment of sympatric species of Ambys- nually. At high elevations, where the environment is more
toma have been interpretad as adaptations to adult sur- certain but colder with a shorter season of activity, fe-
vival (Wilbur, 1977a). According to his analysis of pop- males require 5—6 years to mature and breed every
ulaüons in southern Michigan, Ambystoma tigrinum 2-3 years. Coastal populations of newts, Notophthalmus
deposits eggs in several small clumps, in ponds that are viridescens, live in harsh, unstable environments com-
usually permanent. Larval survivorship is relatively con- pared to inland populations. The latter have a terrestrial
stant and high, but adult survivorship is low. Thus, high eft stage and delay maturity until an age of 4-8 years,
reproductive output is favored, and the species matures whereas in the coastal populations the eft stage is omitted
early and has high fecundity. Ambystoma macu/atum de- and maturity occurs in 2 years. This difference has been
posits eggs in a single mass in semipermanent ponds; interpreted as a high degree of r-selection on coastal pop-
larval survivorship is variable, but adult survivorship is ulations (Healy, 1974); however, the difference could
high. Therefore, it is advantageous for a female to repro- result from proximate environmental effects. In the aquatic
duce many times; females have a relatively low repro- plethodontid Gyrinophi/us porphyriticus, selection has fa-
ductive effort each year but reproduce more times during vored earlier maturity and higher size-specific fecundity
a lifetime and thereby compénsate for uncertain larval in populations at low elevations subject to greater climatic
survivorship. Ambystoma ¡aterale deposits small eggs singly fluctuation than in populations in more certain environ-
in the most temporary ponds. This species has the highest ments at higher elevations (Bruce, 1972a). Populations
reproductive effort relative to body size and has sacrificed of Desmognathus ochrophaeus differ in age at first re-
egg size for increased fecundity. The larvae develop rap- production in contrasting environments (Tilley, 1973). In
idly and metamorphose over a wide range of body sizes— comparison with populations at low elevations, those at
an adaptation to unpredictable environments. Wilbur's high elevations have delayed maturity accompanied by
model applies to populations of A. macu/atum in Con- larger body size and concomitant increased age-specific
necticut, where females breeding in permanent ponds fecundity.
produce more, but smaller, eggs than those breeding in Populations living in a fluctuating environment may be
temporary ponds (Woodward, 1982a). However, Kaplan variable in their life-history strategies. The irregular breeding
and Salthe (1979) showed that smaller salamanders de- cycle of Pseudotriton montanus in the Piedmont of South
vote proportionately more body volume to eggs than Carolina may be an adaptation that favors longevity and
larger salamanders; thus, Wilbur's conclusions are ten- provides for iteroparity while allowing for high fecundity
uous. (Bruce, 1975). In parts of California characterized by a
Similar adaptive modifications exist among hylid frogs variable dry season, the small fossorial salamander Batra-
in humid tropical forests (Duellman, 1978; Crump and choseps attenuatus is highly flexible in its life-history strat-
Kaplan, 1979). In the upper Amazon Basin, most hylids egy (Maiorana, 1976). These salamanders maximize their
breed at ponds that are subject to fluctuation in water reproductive effort per lifetime by regulating clutch size
level. Probably all of the species deposit clutches several and timing deposition according to seasonal fluctuations
times during the year. Species such as Hy/a paruiceps, and available energy.
H. rhodopepla, O/o/ygon cruentomma, O. garbei, and In nearly all amphibian populations that have been
O. rubra deposit relatively large clutches in temporary studied, predation pressure on eggs and larvae is high,
ponds. Others such as Hy/a bifurca, H. sarayacuensis, and juvenile mortality fluctuares more than adult mor-
H. triangu/um, Phy/íomedusa pa//iata, and P. tarsius de- tality. In situations where larval survivorship varíes un-
posit smaller clutches on vegetation over the water. The predictably in time, múltiple small clutches are favored,
eggs of the latter group are larger, have a higher caloric because this strategy decreases the chances of total fail-
contení, and hatch into larger, more advanced tadpoles. ure for a given breeding period. Thus, in such situations,
The deposition of arboreal eggs may be viewed as an selection favors the production of small numbers of off-
adaptation to avoid the uncertainty of the aquatic envi- spring at various times or places, instead of the synchro-
ronment during the period of egg development; further- nous production of a larger number of offspring.
more, the placement of a larger hatchling in the larval However, the reproductive strategies of amphibians are
environment may be advantageous in that the tadpole closely associated with general environmental conditions.
must spend less time there in order to reach metamor- Because of seasonal limitations in températe and wet-dry
phosis. In the species that deposit their eggs on vegeta- tropical regions, breeding patterns are synchronous in
tion, clutch size has been sacrificed for increased egg size. most species. There is limited opportunity for múltiple
 Reproductiva Strategies
clutches in time, but females may scatter their eggs. In températe región may require 2 years. However, the sec- 49
aseasonal, humid, tropical environments, breeding can ond frog may been inactive for 6 months of each year;
be more or less conünuous, and múltiple small clutches therefore, in terms of actual time of active feeding and
provide a means of reducing reproductivo effort per clutch growth the two frogs are the same age. Furthermore, the
and at the same time enhancing survivorship of the early reproductive life span must be considered.
stages by placing eggs in different places at different times. Obviously, reproductive strategies are compromises
One aspect of time to maturity often is overlooked. In among various selective pressures. Consideration of the
amphibians, absolute age is not a reasonable criterion interrelationships of selection for early versus late matu-
when comparing tropical with températe species. A frog rity, more and smaller versus fewer and larger eggs, and
in an equatorial rainforest may reach sexual maturity in low versus high investment per egg (Fig. 2-20) presents
1 year, whereas a frog of similar size in a midlatitude a general view of reproductive strategies. A shift into the
área A-C-E involves an increase in clutch size brought
about by low investment per egg and late maturity. In
the opposite área (B-D-F), clutches are small with a high
investment per egg in early-maturing species. This model
is applicable to comparisons among groups of closely
related species or populations of the same species exist-
ing under different selective pressures. Likewise, we can
compare diverse groups of amphibians in a general way.
Viewing all amphibians in the model, we see that not all
of the áreas are filled equally. The área B-D-F is occupied
by dendrobatid frogs and Eleutherodactylus, among others,
whereas terrestrial plethodontid salamanders tend more
toward the área B-D-E. Most Hyla and Bufo and deser-
ticolous anurans like Scaphiopus are in the área A-C-F,
whereas Rana tends more to the área A-C-E with tropical
species in A-C-F and some stream-breeding species in
^ Fewer, B-D-E. As a group, Ambystoma are in the área B-C-F,
-Eggs Larger
Smaller
and large aquatic salamanders (Cryptobmnchus and
Figure 2-20. Relationship among number and sizes of eggs, Necturus) are in the área B-D-E. The relative positions
investment per egg, and demography. Line A-B is the combination of various species with respect to aspects of their repro-
oí egg number and egg size, line C-D is the energy allocation per
egg, and line E-F is the combination of age at first reproducción ductive strategies are an indication of the kinds of past
and reproductive lite span. See text for further explanation. and present selective pressures on the species (Fig. 2-21).

Figure 2-21. Three-dimensional plot

of factors in life history strategies.
Numbers are salamanders:
1. Cryptobranchus alleganiensis,
2. Siren intermedia, 3. Trituras
milgarts, 4. Necturus maculosus,
5. Ambystoma tigrinum,
6. Rhyacotríton olympicus,
7. Desmognathus ochrophaeus,
8. Hemidactylium scutatum,
9. Bolitoglossa rostrata,
10. Plethodon cinéreas,
11. Plethodon glutinosas.
Letters are anurans: A. Ascaphus
truei, B. Bambino bambino,
C. Hymenochirus boettgeri, D. Bu/o
canoras, E. Bu/o quercicus, F. Bu/o
valliceps, G. Hyla cinérea, H. Hyla
cracifer, 1. Hyla rosenbergi, J. Rana
aurora, K. Rana catebeiana, L. Rana
pretiosa, M. Rana sylvatica,
N. Megistototis lignarias,
O. Phyllobates terribilis,
P. Eleutherodactylus planirostris. All
Smaller-» Clutch Size (Log) -•-Larger are mean valúes.
LIFE HISTORY
50 The adaptive radiation of reproductiva strategies is among living anurans that have terrestrial eggs, some of
closely associated with the environmental histories of the which hatch as tadpoles that complete their development
groups. The life histories of generalized hynobiids may in water and others that do not feed and complete their
be viewed as the primiüve reproductive pattern in sala- development in the nest. In many cases these modes are
manders. The deposiüon of numerous small eggs in ponds associated with obligatory parental care. The evolution
with subsequent ferülization limited the dispersal of sal- of these reproductive modes was possible in environ-
amanders. The adaptation of placing eggs in streams still ments such as lowland tropical rainforest or humid mon-
had restrictions, because of inadequate means of fertil- tane forest having high atmospheric humidity. In the lat-
ization, until the development of the spermatophore, which ter, frogs also developed modifications of oviposition and
allowed for the deposiüon of eggs on preexisting sperm. larvae for stream habitáis.
Subsequent evolution of the female behavior in picking Dispersal into seasonally dry tropical regions and into
up the spermatophore opened a vast array of reproduc- températe regions necessitated other kinds of modifica-
tive possibilities—increased assurance of fertilization of tions in the reproduction of anurans. Sexual cycles be-
eggs no matter where or when they were deposited. With came seasonal, and innate timing was required so that
the advent of the spermatophore, sexual cycles could the frogs were ready to breed when the environment
vary independently of breeding patterns, thereby result- permitted. In predictably seasonal áreas, the most nota-
ing in adaptation to diverse environments. Occupation of ble strategy is to deposit many small eggs that develop
moist, montane habitáis probably was a precursor to the rapidly into small offspring that can leave water at an
deposition of terrestrial eggs with concomitant female at- early age. In áreas where temporary ponds are of longer
tendance. We can see in living species of plethodontids duration, reproductive effort can be divided into more
a continuum from small aquatic eggs that hatch into lar- than one clutch. The habit of depositing eggs in a foam
vae requiring many months to metamorphosis, through nest is another adaptation to avoid desiccation of the
larger eggs with short larval spans and still larger eggs eggs. In températe regions where reproduction is limited
with nonfeeding larvae, to large terrestrial eggs that de- by temperature, the general trend is to retain the gen-
velop directly into small salamanders. Only with internal eralized reproductive mode of egg and tadpole devel-
fertilization was it possible for ovoviviparity and viviparity opment in ponds. The major variation on this theme re-
to evolve in salamandrids. It is surprising that these modes lates to size and fecundity, that is, large females depositing
are so limited in salamanders. many thousands of small eggs versus fewer larger eggs
Somewhere in their early evolution, caecilians presum- resulting in larger hatchlings that spend less time in the
ably evolved internal fertilization. Their subsequent re- water.
productive adaptations have involved the specialization Within these general evolutionary trends in anurans
of viviparity, which is associated with early maturity, long there are many specializations restricted to a few species
development time, low fecundity, and long adult surviv- (e.g., stomach brooding and carrying tadpoles in pouches),
orship. and there are some deviations that are counter to general
Anurans presumably originated and underwent their trends (e.g., nonfeeding tadpoles in terrestrial foam nests
major adaptive radiation in the humid tropics. The prim- in humid regions). However, the major trend is clear—
itive life history probably was the deposition of a single increased terrestriality. The available information on anu-
clutch of eggs in ponds, where larvae developed. Per- ran life histories clearly shows that this evolutionary trend
manent aquatic sites harbored many predators on both occurred independently in many groups of anurans. De-
eggs and larvae. Modifications in life histories to avoid spite the general absence of internal fertilization, many
this predation included the placement of eggs in tem- anurans have succeeded in divorcing their life histories
porary ponds, which provided a highly uncertain envi- from the aquatic environment.
ronment for eggs and larvae. Deposition of numerous The evolution of diverse reproductive strategies in am-
smaller clutches enhanced the probability of loss of all of phibians is an example of many success stories. Many
the eggs. By placing eggs on vegetation above ponds, evolutionary experiments in amphibian life histories
survivorship of the eggs was increased, and by increasing probably have been abandoned and their proponents are
egg size (at the expense of the number of eggs), a greater now extinct. A few probably remain to be discovered.
proportion of the development took place in the egg, The important thing is that amphibians have adopted
thereby shortening the time that the larva must spend in diverse life- history strategies contingent upon their en-
an uncertain environment. Escape from the exigencies of vironmental regimes, and that the diversity of these strat-
the aquatic environment was accomplished by packaging egies among the group as a whole and their flexibility
reproductive energy into a few large eggs that provided within species and even within populations are reflected
the caloñe contení necessary to carry the egg through to in the evolutionary and ecológica! diversity of amphib-
metamorphosis without depending upon a feeding larval ians, the pioneers of the terrestrial environment.
stage. Many intermedíate evolutionary steps are found
 CHAPTER 3
fF* a not small enough to eat ñor ¡arge
í to eat you, and does not pul up a
c about it, mate with it.
David L. Jameson (1955b)

s 'uccessful propagaüon of an individual's genes de-

pends on the location of potenüal mates, stimulation of
mates, selection of breeding site, fertilization of the eggs,
congregation of individuáis at particular breeding sites.
This also may be true for anurans that live along moun-
tain streams in cloud forests; the frogs are there through-
and development of the eggs and young. Location of out the year. On the other hand, most amphibians that
mates may be by visual, olfactory, auditory, or tacüle deposit eggs in (or above) ponds and some that breed
means, or a combinatíon of these. In some vertebrales, in streams congrégate for breeding. In some instances,
mating occurs with littíe or no specialized behavior, whereas migrations to breeding sites cover distances up to several
in other groups, especially those characterized by com- kilometers. The factors that initiate these movements have
píex, social interactions, diverse kinds of courtship are an been discussed in Chapter 2, but here the emphasis is
integral part of mating and mate selecüon. Generally, on the methods used by amphibians to lócate breeding
during courtship, males are the more aggressive sex, and sites, including auditory, olfactory, and visual cues, as
their courtship activities depend on female response. well as geotactic and hygrotactic stimuli.
In Chapter 2, the evolution of reproductivo strategies
was examined; here the concern is more with the inter- Auditory Cues
actions among individuáis: (1) How do individuáis lócate Vocalizations clearly attract anurans to breeding sites, and
breeding sites and mates? (2) What are the courtship there is growing experimental evidence to support au-
behaviors? (3) How are mates selected, and what factors ditory orientation in anurans (see Chapter 4 for details
contribute to mating success? (4) Where are eggs de- of auditory reception and response). Receptive females
posited and how are they fertilized? These various as- and males of Bufo terrestris responded positively at dis-
pects of reproducüon differ not only along taxonomic tances up to 40 m to a recording of a conspecific chorus
unes and in different environments but also to some de- (Bogert, 1960). Male chorus frogs, Pseudacris triseriata,
gree at different densities within populations. orient at distances of 50-75 m to natural and recorded
choruses (Landreth and Ferguson, 1966). An advertise-
ment cali is absent in B. bóreas, but males and females
LOCATION OF BREEDING SITE moved toward a recording of male reléase calis at night
Many amphibians, especially those that have terrestrial (Tracy and Dole, 1969).
eggs, carry out courtship and reproductivo activities within Although vocalization may play a role in directional
their normal home ranges; in these species, there is no movements to a breeding site in many kinds of anurans,
51
LIFE HISTORY
52 other factors may predomínate. Certainly the first calling Ferguson, 1970). The pineal body has been shown to
individuáis must lócate the site by other cues. Further- be a funcüonal photoreceptor, and covering the pineal
more, movements toward a breeding site have been ob- área results in disorientaüon (K. Adler, 1970; D. Taylor
served at distances far beyond the presumed audible range and Ferguson, 1970).
of the chorus. Most migrations take place on rainy or overcast nights,
Although initial orientation before sunset may influence
Olfactory Cues the direction of migraüon, celestial cues probably are not
Considerable evidence supports the use of olfaction in important in long-distance migrations by amphibians in
migratíon to breeding sites by anurans and salamanders. one night.
Odors given off by algal blooms are suspected to be the
major factor in the initiation and orientation of breeding Other Factors
migrations in Rana tempana (R. Savage, 1961). Martof Geotactic and hygrotactic responses may be important in
(1962a) placed Pseudacris tríseriata in a T-maze and found migrations, especially because breeding sites situated in
that 71% of the individuáis moved toward odors from depressions usually have a humidity gradient. However,
the breeding site rather than toward odors from upland such factors can be of little importance in long-distance
forest. Green frogs, R. clamitans, demónstrate direcüonal migrations during which animáis move uphill or away
movement to breeding sites at distances up to 550 m; from one watershed to another, or cross open fields be-
this homing response is not impaired significantly by the tween forested áreas. Furthermore, individuáis often en-
absence of auditory, visual, hygrotactic, or geotactic stim- ter and leave a breeding site by the same path (Shoop,
uli, but it is reduced significantly by the ablation of the 1965a, 1968; Hardy and Raymond, 1980) or return to
olfactory receptors (Oldham, 1967). Odor seems to be the same site year after year (Twitty, 1961; Oldham, 1967).
the major factor in orientation and movement in R. pi- A strong attachment to a particular breeding site is known
piens; blinded individuáis orient and move toward breed- in several species, and cases exist of individuáis returning
ing sites, as do normal frogs at distances up to 800 m to the site of a pond after it has been obliterated, as for
(Dole, 1968). Bufo bufo (Heusser, 1960) and Ambystoma talpoideum
Extensive experiments on the terrestrial newt, lancha (Shoop, 1968). Likewise, efts of Notophthalmus virides-
rivularis, indícate that odor is an important but not ex- cens, after 2 to 4 years on land, usually return to the
clusive factor in orientation (Twitty, 1961, 1966; Twitty pond where they developed as larvae, even though other
et al., 1967). Newts that were displaced 3-4 km returned ponds are available (Hurlbert, 1969), and adults retum
to the horne segment of the breeding stream before or to the same ponds yearly for breeding (Gilí, 1978).
during the next breeding season, and some individuáis Although one factor may predomínate in the orienta-
displaced 8 km were found in the original breeding stream tion of a given species under certain circumstances, dif-
the next year. Newts normally confine their breeding mi- ferent factors may be important under other conditions,
gration to one watershed, so homing from points beyond or one set of cues may replace another during long-dis-
the stream system cannot be based on familiarity with tance movements. Thus, species of anurans making long-
the sites of reléase. Blinded newts home successfully, but distance migrations may depend initially on celestial or
those in which a secüon of the olfactory nerve had been olfactory cues unül within auditory range of a breeding
removed did not home successfully until the nerve re- chorus. Also, some species may utilize several cues si-
generated (D. Grant et al., 1968). Similar experimental multaneously; no single sensory cue (olfactory, visual,
results were obtained with normal, blinded, and olfac- auditory, geotactic, or hygrotactic) is essential to orien-
torectomized Plethodon jordani (Madison, 1969). tation in Bufo bufo, but each may contribute to orien-
tation (Heusser, 1960). Thus, a wide range of cues may
Visual Cues be important in movements to breeding sites, but the
Amphibians can orient to a particular compass direction relaüve contributíon of each of these factors to breeding
when provided with celestial cues. An interna! clocking migrations is poorly understood.
mechanism presumably compénsales for variatíons in the
posiüons of the celestial bodies (Ferguson, 1967). The
sun seems to be the most commonly used celestial cue, SECONDARY SEXUAL CHARACTERS
but ability to orient to stellar patterns or the moon is In addition to the reproductíve organs and their associ-
indicated in some frogs (Acrís gryllus and Rana cates- ated tracts, external sexual differences exist in most am-
beiana). Most demonstrations of this kind of mechanism phibians, including size, glandular development, skin tex-
have dealt with Y-axis orientation, in which a displaced ture, dermal ornamentatíon, vocal sacs, and coloraüon.
animal orienta in a direction at right angles to the home Some differences persist throughout adult life, but others
shoreline. The fact that blinded animáis can orient to develop in response to gonadotropic hormones and
celestial cues indícales that extraopüc receptors are im- therefore are present only during the active reproductíve
portant (Ferguson and Landreth, 1967; D. Taylor and cycle. Some structures are used in courtship and others,
 Courtship and Mating
for holding the pair in an embrace during mating or ovi- 53
position. The nature of sexually dimorphic characters is
sufficientíy different in the three groups of amphibians
that the groups are best treated separately.

Caecilians
External sexual differences are lacking in most caecilians.
In some aquatic typhlonectids, the anal región of the
inale is modified to form a circular depression, which E.
Taylor (1968) thought could serve as a suction mecha-
nism to facilítate copulation in water. However, in ob-
served copulations in two typhlonectid genera—Chtho-
nerpeton (Barrio, 1969) and Typh/onectes (Murphy et
aL 1977)—the male is not attached to the female other
than by the insertion of the phallodeum. Nevertheless,
strong sexual dimorphism exists in the anal región of Figure 3-1. Cloacal regióos of Ambystoma jeffersonianum
typhlonectids of the genus Potomofyphlus; E. Taylor showing swollen glandular área around vent and cloacal papillae in
(1968:18) suggested that "this área seemingly becomes male (left) and unswollen cloacal área of témale (right).
a clasper, in the males being enlarged and capable of
partly or wholly grasping this área in the females." This
has yet to be confirmed by observaüon.

Salamanders
Sexual dimorphism in size of most salamanders is not
yeat. Usually females are slightly larger-than males, but
the sexes are about the same size in many species. Males
are larger than females in a few species (Shine, 1979).
Generally, larger body size in females has been thought
to be related to egg-carrying capacity, because there is a
positive correlation between female body size and clutch
size. Shine (1979) interpreted large body size in males
as an advantage for combat between males. Figure 3-2. Sexual differences in fin structure and coloration in
During the breeding season, the vents of males be- newts, Trituras cristatus; male above, female below.
come swollen (Fig. 3-1); lobes form lateral to the vent in
ambystomatids and posterior to the vent in some pleth-
odontids. The swelling results from enlargement of the ing. In Triturus this habit is combined with the develop-
cloacal glands; the villi of the glands are visible in the ment of bright colors, especially on the fins, during the
cloacal aperture of some species. The enlargement of the breeding season; thus, the increased surface área and
cloacal glands is controlled by testicular hormones (Noble more extensive coloration seem to have coevolved as
and Pope, 1929). effecüve means of species recognition and provisión of
Males and females of some salamandrids, especially visual, chemosensory, and tactíle cues during courtship.
Tarícha and Cynops, have rough skin when not breed- Although some workers have indicated an increase in
ing, but develop smooth skin during the breeding season. color intensity, such as the spots in male A. maculatum
Presumably the skin texture funcüons in recognition of and A. tigrinum, there is no evidence that these colors
potentially receptive mates in these salamanders, in which are important in sexual recognition. However, during the
many males congrégate around and attempt to grasp a mating season, male Hynobius nebulosus develop a white
female. guiar patch, which is exposed by lifting the head and
Males of some aquatic salamanders, and also males of pulsating the throat in the presence of a female (Thorn,
terrestrial salamanders that breed in water, especially 1967).
ponds, develop more extensivo caudal and (in newts) Males of plethodontids, ambystomatids, and some sal-
dorsal fins during the breeding season. This characteristic amandrids develop courtship glands (Fig. 3-3). These were
is most notable in Trituras (Halliday, 1977) (Fig. 3-2), termed "hedonic" glands by Noble (1927a) and most
but also occurs in others, such as Notophthalmus viri- subsequent authors, but as noted by Arnold (1977:152):
descens (Bishop, 1941) and Ambystoma talpoideum "Whatever functions these glands have, we will never
(Shoop, 1960). The fins in Ambystoma appear to func- know if they are hedonic (pleasure giving)." A series of
tion in creaüng disturbances in the water during tail-wav- genial glands is present in the temporal región of the head
LIFE HISTORY
54

Figure 3-3. Head glands of male salamanders.

A. Genial glands on side of head of
Notophthalmus viridescens. B. Diffuse
submandibular glands of Taricha torosa.
C. Mental gland of Pseudoeurycea smithii.

in male Notophthalmus (Hilton, 1902), and other glands

are present on the side of the neck and in the scapular
región in Cynops pyrrhogaster (Tsutsui, 1931). Subman-
dibular glands are present in male Taricha (R. Smith,
1941). Most male plethodontids have circular mental
glands on the chin (Trufelli, 1954). Glands also are present
on the sides of the head in some plethodontids (Noble,
1929b) and on the base of the tail and/or on the pos-
terodorsal part of the body (Baird, 1951). Glands at the
base of the tail also are known in some Ambystoma
(Shoop, 1960). All of tríese glands come in contact with
the female during courtship. The development of at least
the mental and body glands is influenced by testicular
hormones (Noble, 1931a; Sever, 1976).
Plethodontid salamanders exhibit sexual dimorphism
in the number, size, and structure of the premaxillary
teeth. In males, these are elongate, even protruding
through the lip (Fig. 3-4). In males of Desmognathus and
Eurycea, the premaxillary teeth are monocuspid, at least
during the mating season (Stewart, 1958); females and
Figure 3-4. Adult male of Pseudoeurycea bellü in breeding
nonbreeding males have bicuspid teeth. The develop- condition showing enlarged cirri and elongate premaxillary teeth
ment of elongate, monocuspid teeth is mediated by tes- protruding through upper lip.
ticular hormones (Noble and Pope, 1929). During court-
ship the male uses the elongated premaxillary teeth to
deliver secretíons from the mental glands (Arnold, 1977). and the forelimbs of Pleurodeles and Taricha, and on the
Plethodontids also have a pair of nasolabial grooves; chest and forelimbs of Onychodacty/us in the breeding
during the breeding season the margin of the lip encom- season (Fig. 3-5). Keratinized tubercles also appear on
passing the terminus of each groove becomes elongated the venter in Taricha. These keratinized structures func-
into a cirrus in male plethodontines, but the nasolabial tion in maintaining a grip on the female.
protuberances remain enlarged throughout the year in
bolitoglossines. In male Ensatina, the entíre upper lip be- Anurans
comes enlarged in the breeding season. Presumably the As in salamanders, female frogs usually are larger than
enlarged sensory tracts facilítate olfactory trailing of fe- males, and sexual size dimorphism is great in some frogs.
males by males and avoidance of tracts made by other Females with body lengths 1.5 times the lengths of males
males (R. Jaeger and Gergits, 1979). are common in Eleutherodactylus; in some Rana (e.g.,
In those salamanders having prolonged periods of cap- R. andersonii), males are only about half the length of
ture, nuptial excrescences, consistíng of keratinized epi- females (Liu, 1936). However, in some species, males
dermis, appear on the inner surfaces of the limbs of males are equal to or slightly larger than females. Shine (1979)
during the mating season; also, the rnusculature of the analyzed size dimorphism and found significant correla-
appropriate limbs becomes hypertrophied. Nupüal ad- tions between large size in males (relative to females) and
spersitíes are present on the hindlimbs of Notophthalmus, (1) male-male combat and (2) presence of tusks or spines
 Courtship and Matíng
in males; he concluded that selection favored larger males lenid frogs. Limited observations (McDiarmid, 1975; 55
in species having aggressive behavior. Duellman and Savitzky, 1976) indícate that male-male
combat in species of Centrolenella involve grappling and
hooking of an opponent with a humeral spine. The Pap-
Spines and Tusks. Spines or tusks are present in males uan hylid Nyctimysíes humeralis also has humeral spines
of many species (Fig. 3-6). The best-documented cases in the male (Zweifel, 1958), and perhaps it too engages
of the use of spines in combat is in the gladiator frogs of in combat.
Ihe Hy/a boans group, in which males defend their nests Sharp odontoids or tusks on the lower jaw occur in
by grappling. Fatal wounds are inflicted by puncturing both sexes of several kinds of frogs, especially camivo-
opponents with the sharp prepollical spines during wres- rous types such as Ceratobatrachus, Hemiphractus, and
tfing bouts; this combat has been observed in Hy/a faber Pyxicepha/us. Tusks are present in both sexes of the Bra-
(B. Lutz, 1960) and H. rosenbergi (Kluge, 1981). Also, zilian hylid Phy/íodytes íuteo/us; the much larger tusks of
use of prepollical spines has been observed in aggressive males are used in biüng other males during combat
bouts between males of Leptodacty/us pentadacty/us (Weygoldt, 1981). Similarly, the tusks are much larger in
(Rivero and Esteves, 1969). Males of the Hy/a a/bom- males than in females of Adelotus breuis, an Australian
arginata, granosa, and miliaria groups also have project- myobatrachid. Males cali from the midst of floating foam
ing prepollical spines, as do males of the microhylid Ho- nests; the sexual dimorphism suggests that males may
pfophryne rogersi, but there are no observations of combat use the large tusks in defense of their nests. A similar
in these frogs. Single or bifid prepollical spines are present dimorphic condition exists in the African ranid Dimor-
in both sexes in species of P/ectrohy/a, but they are best phognathus africanas, in which the maxillary teeth in fe-
developed in males, which are larger than females. Many males are moderately long and bicuspid; those in males
adult male P/ectrohy/a have numerous scars, perhaps re- are long and monocuspid. However, no information ex-
sutóng from wounds received during combat with other ists on differential use of teeth. Three species of the Ori-
males. Projecüng spines from the proximal end of the ental pelobatíd genus Leptobrachium are unique in hav-
humerus are present in males of many species of centro- ing a row of cornified labial spines in males (Liu, 1950;

Figure 3-5. Nuptial excrescences in

salamanders. A. Forelimbs of Pleurodeles waltl.
B. Hindlimbs of Notophthalmus viridescens.

Figure 3-6. Spines on limos of male anurans.

A. Prepollical spine of Hyla rosenbergi.
B. Humeral spine of Centrolenella buckleyi.
Bones are stippled.
LIFE HISTORY
Dubois, 1980). The presence of spines (Fig. 3-7), in com- In some frogs, they extend distally on the thumb and also
bination with the larger size of males compared with fe- may be present on the median or dorsal surfaces of the
males, suggests the use of the spines in aggressive be- second and third fingers and/or on the ventromedial sur-
havior. face of the forearm; Bombina also has nuptial excres-
cences on its feet.
Nuptial Excrescences. The most notable secondary Most frogs that amplex on land or on vegetation either
sexual characters in anurans, except for vocal sacs, are lack or have minimally developed excrescences. Nuptial
the nupflal excrescences on the prepollices of males dur- excrescences are nearly universal in frogs that amplex in
ing the breeding season. It has been well established that water, and they are best developed in species that breed
the development of nuptial excrescences is influenced by in streams. Furthermore, males of many stream-breeding
testicular hormones (Greenberg, 1941; Cei, 1944), and species have large clusters of spines on the prepollex,
seasonal variation in development as correlated with re- and some have excrescences or spines on the chest (Fig.
productive activities has been demonstrated by Inger and 3-8). Pectoral spines also are present in some large spe-
Greenberg (1956, 1963). The nuptial excrescences con- cies of pond-breeding Leptodacty/us. Extensively devel-
sist of modified dermal and epidermal tissues. The outer oped nuptial excrescences commonly are accompanied
layer of the corium has small, conical protuberances, over by greatly hypertrophied forelimbs (Fig. 3-9). The in-
which the stratum germinativum of the epidermis is thick- creased muscle masses are anchored to broadened flanges
ened into a cornified covering which may be simply ru- on the humeáis, as in some species of Leptodacty/us
góse or modified into cones or spines that usually are (J. D. Lynch, 1971) and hylids such as Plectrohyla
densely pigmented with melanin. Large mucous glands (Duellman, 1970). Nuptial excrescences obviously are
are imbedded in the corium. If present, these excres- associated with amplexus, but they also may play a role
cences always are on the median surface of the prepollex. in male-male combat. The extent and spinosity of the
excrescences seem to be correlated with the difficulty of
maintaining amplexus, which presumably is most difficult
in torrential streams. Nuptial excrescences also may be
important in males holding on to mates when other males
are trying to dislodge them (Wells, 1977a). Pernales of
/nsuetophrynus acarpicus, a stream inhabitant in south-
ern Chile, have keratínized excrescences that are less de-
veloped trian those in males (Diaz et al., 1983).
Pernales of limnodynastine myobatrachids that have
aquatic foam nests develop broad lateral fringes on the
fingers during the breeding season (Fig. 3-10). These
fringes provide a much greater surface área to the hands,
which are used in paddling movements for stirring water
and spawn into a foam nest. Males lack the fringes, but
males of some species have a knoblike medial projection
on the distal end of the penultimate phalange of the first
finger.

Other Phalangeal Structures. The funcüon of other

secondary sexual characters of the extremities is not known.
Males of arthrolepüne ranids have exceedingly long third
fingers. In Cardioglossa, there are 15 to 20 large dermal
denudes on the median surface of the finger; fewer and
smaller denudes are present in/Arthro/eptis, and denudes
are absent in Schoutedenella (Perret, 1966). Males of the
hyperoliid Acanthtxalus spinosus have many cornified
spines on the posteroventral surface of the tarsus and
also have much larger discs on the fingers than do the
females (Perret, 1961). In males of some species of Co-
lostethus, the distal part of the third finger is noticeably
broadened; this may be associated with cephalic am-
plexus. Males of the Oriental microhylids Kaloula rugi-
fera, macroptica, and verrucosa have 3 to 10 tubercles
on the dorsal surface of the üp of each finger. Each tu-
Figure 3-7. Tusks and spines of male frogs. A. Enlarged
mandibular odontoids of Adelotus breáis. B. Labial spines of bercle is supported by a bony projection from the ter-
Leptobrachium (Vibríssaphora) boríngii (modified from Liu, 1950). minal phalange. Females have barely distinguishable ir-
 Courtship and Mating
57

Figure 3-8. Nuptial excrescences in

breeding male frogs. A. Rana
macúlate. B. Bufo bufo. C.
Ptychohyla spínípollex. D. Bambino
oríentalís. E. Leptotlactylus
pentadactylus. F. Hyla ármate.
G. Scutiger adungensis (modified
from Dubois, 1979a). All are ventral

Figure 3-9. Hypertrophied forelimb of male Leptodactylus Figure 3-10. Sexual differences in hands of Limnodynastes peroni,
pentadactylus (left) and normal forelimb of female (right) and showing projection on first finger of male (left) and dermal fringes
extensive development of flanges on humerus of male as compared on fingers of témale (right).
j. ¡th female.
LIFE HISTORY
58

Figure 3-11. Secondary sexual

characters of hands and feet of male
anurans. A. Swollen third finger in
Colosthethus nubicola. B. Elongate
third finger with lateral denticles in
Cardioglossa cyanospila.
C. Elevations on dorsal surfaces of
second finger in Kaloulu verrucosa
(redrawn from H. Parker, 1934).
D. Tarsal spines in Acanthixalus
spinosus (adapted from Perret, 1966).

regularles on the fingere (H. Parker, 1934; Liu, 1950)

(Fig. 3-11).

Glands. Glands develop on the ventral surfaces of

breeding males in many kinds of anurans (Figs. 3-12, 3-
13). Abdominal glands are present in many microhylids
that are excessively rotund-bodied (e.g., Breviceps, Gas-
trophryne, Kalouh); these glands secrete an adhesive
substance that helps the male maintain amplexus (Con-
away and Metter, 1967; Jurgens, 1978). At least in Brev-
iceps gibbosus, females have similar adhesive glands on
the dorsum (Visser et al., 1982). The function of the other
ventral glands in male frogs is unknown, but because
they are in contact with the female during amplexus, it
Figure 3-12. Glands of male frogs. A. Mental gland of Kassina
is assumed that the secretions from these glands have senegatensís. B. Pectoral glands of Leptopelis karissimhensis.
some stimulating effect on ovulation or ovipositíonal be-
havior by the female. Mental (guiar) glands of various
shapes are present in all genera of hyperoliids, except
Leptopehs, and in members of the Neotropical Hyla bo-
gotensis and Australian Litaría atropa groups; these glands
seem to be present throughout the year in most species.
Extensive, thickened, and pigmented ventrolateral glands
develop in males of all species of the Middle American
Ptychohyla. Males of at least some species of Leptopelis
have a pair of pectoral glands or a single transverso gland
in the pectoral región; these glands consist of groups of
glandules identical to those forming the nuptial pads (K.
Schmidt and Inger, 1959). Round or ovoid "femoral"
glands are present on the ventral surfaces of the thighs
of some African ranids (Petropedetes, Phrynodon, and
some species of Phrynobatrachus) and Madagascaran Figure 3-13. Glands of male frogs. A. Abdominal gland of
ranids (Laurentomantis and some species of Mantidac- Kaloula verrucosa. B. Ventrolateral glands of Ptychohyla
schmtdtorum. C. Femoral glands of Mantidactylus pseudoasper.
tylus). A postaxillary gland is present in breeding males
of the pipid genera Hymenochirus and Pseudhymeno-
chirus. Other glands develop in breeding males of some gland posterodorsal to the axilla in Rana adenop/eura
ranids; these include glands on the dorsal surface of the and its relatives. Males of many hyperoliids have glands
hand in Dimorphognathus and Hemisus, "humeral" glands on the inner surface of the forearms.
on the dorsal surface of the arm in some Rana and Hy-
larana (Fig. 3-14), a gland on the snout of Rana macro- Skin Texture. Sexual differences in skin texture are
dactyla (also in Polypedates dennysij, and a large lateral common in toads and also occur in some other anurans.
 Courtship and Mating
fa the toads of the Bufo spinulosus group, males have the breeding season (Perret, 1966). Also, small spicules 59
•ore numerous and cornified tubercles dorsally than do develop on the dorsum and/or venter in some species of
fanales (Fig. 3-15). The same is true in Bufo regularte, Ptychadena, Rana, and Gastrophryne during the breed-
Ijmnodynastes spenceri, Megistolotis lignarius, and Hel- ing season. In Scutiger mammatus, females have rugóse
aaporus australiacus, in which the cornified spines are skin on the dorsum and flanks (Liu, 1950). Any of these
cspetially evident in the breeding season. Males of some dermal characters may be importan! in sex recognition
CfTÉrolenella have spicules on the dorsum. On the other by tacüle means. However, the presence of small tuber-
land. males of Bu/o bu/o and B. Jciso/oensis, among cles on the margin of the jaw in some species of Phry-
ahers. have relatively smooth skins with only low, flat- nobatrachus may have some other function.
tened tubercles, in contrast to the more tuberculate skin The most notable integumentary modifications occur
al females. Males of the Neotropical tree frogs of the in the African ranid Trichobatrachus robustus (Fig. 3-16).
gemís Osteocephalus have tuberculate skin, whereas the During the breeding season, males have long, hairlike
skin of females is essentially smooth; the size and density projecüons on the flanks and thighs; these projecüons
of íhe tubercles are species-specific (Trueb and Duell- consist of vascularized epidermis (Noble, 1925a). Males
tnan. 1971). Males of the hyperoliid Afrixalus fulovittatus are known to sit on clutches of eggs in streams (Perret,
have finely tuberculate skin on the dorsum only during 1966), and presumably the "hairs" function to increase
cutaneous respiraüon, thereby allowing males to remain
under water for long periods of time.

Cloacal Modifications. The most notable modifica-

tion of the cloaca is the cloacal extensión or "tail" of
male Ascaphus truei, which is ¡nserted into the cloaca of
the female. Males of the small African bufonid Merten-
sophryne micranotis have protruding spiny venís; Gran-
dison (1980b) postulated that these spines fit into furrows
in the female's vent and that fertilizatíon is internal. In
most anurans, the opening of the vent is bordered by
papillae or dermal folds, and there is no evident sexual
dimorphism in the shape or position of these structures
or of the direction of the opening. However, in Kossina,
dermal flaps border the vent in females; perhaps these
flaps function in the dispersal of the eggs as they leave
the vent. In female Pipa, the vent of the female becomes
greatly swollen just prior to oviposition.

Coloration. Males of many species of frogs develop

pigmented vocal sacs during the breeding season, which
may extend throughout the year. In Bu/o the throats
become gray or black, whereas in many small Hyla they
become bright yellow. In some species of Colostethus
the throat becomes black, but because melanin is less
dense posteriorly the belly has a grayish hue; in others
Figure 3-14. Humeral gland on arm of male Hylarana albolabris. the throat is yellow or white. Many species of toads ex-

Figure 3-15. Sexual differences in

skin texture in Bufo spinulosus; male
(left), female (right). Photos by W. E.
Duellman.
LIFE HISTORY
60 parviceps group have a broad diagonal palé mark dorso-
laterally on the body; this mark is absent in males (Duell-
man and Crump, 1974). The ontogeny of sexual dichro-
matísm of Bu/o canorus was documented by Karlstrom
(1962); juveniles of both sexes are spotted, but in older
males there is a reduction of spotüng, while in females
the spots become accentuated with age. The seasonal
development of throat color in males is under the control
of testicular hormones (Greenberg, 1942), but the causes
of continuous sexual dichromatism are as unknown as
the functions. Male Co/ostethus trinitatus change from
palé brown to black when calling; this color change oc-
curs in a matter of 1 to 10 minutes, as does the reverse
change at the end of calling (Wells, 1980b).

Tympanum. In most anurans, the tympanum is rela-

tively the same size in both sexes or slightly larger in
females; however, in some ranids—species of Rana (e.g.,
R. catesbeiana and R. clamitans), Ptychadena, Conraua,
and Hylarana— the tympanum is notably larger in males.
In some species of the ranid genus Petropedetes the col-
umella protrudes through the tympanum in males (Fig.
3-17). The reasons for these differences are unknown.
There are no correlations between tympanum size and
auditory sensitivity in Rana catesbeiana (Frishkopf et al.,
1968). The condition in Petropedetes would diminish the
vibratory capacity of the tympanum and thus would re-
duce sensitivity to higher frequencies.

Linea Masculinea. A curious sexually dimorphic

Figure 3-16. Breeding male of Trichobatrachus robustas showing
character in some frogs is the linea masculinea, which
hairlike dermal appendages. From Boulenger (1902). consists of bands of fibrous connective tissue extending
the entire length of both layers of the dorsal and ventral
edges of the m. obliquus (Liu, 1935a). Lineae masculi-
neae are known in males of many species of Rana and
Occidozyga and in such diverse frogs as species of Me-
gophrys, Hyla, Plectrohyla, Polypedates, Philautus,
Phrynobatrachus, Kaloula, Kalophrynus, and Microhyla
(Liu, 1936; K. Schmidt and Inger, 1959; Duellman, 1970).
The function of this connective tissue and why it is present
in some species and absent in congeners are completely
unknown. In gonadectomized male Rana pipiens, the li-
nea masculinea remained unchanged, thereby suggesting
that its maintenance is not dependent on testícular hor-
mones (D. Davis and Law, 1935).
Figure 3-17. Head of male Petropedetes newtoni showing the
columella protruding through the tympanum.
COURTSHIP BEHAVIOR
The locatíon and stímulation of potential mates are ac-
hibit constant color differences between adult males and tivities primarily associated with male amphibians, but
females. Usually the females are more boldly marked, as some recent evidence shows that in some species females
in the mottling of Bu/o canorus, dorsolateral stripe in B. also play an active role. Courtship in salamanders has
preussi, and broad green middorsal mark in B. marmo- been reviewed by Joly (1966), Salthe (1967), Organ and
reus. Bufo periglenes displays striking sexual dimorphism Organ (1968), Salthe and Mecham (1974), Arnold (1976,
in coloraüon; males are uniformly bright orange, and fe- 1977), and Halliday (1977); courtship in frogs has been
males are dark and rather dull except for red spots (J. reviewed by Wells (1977a, 1977b). The behavior is no-
Savage, 1967). Males of Scaphiopus couchii are plain, tably different in the three groups of living amphibians,
and females are mottled. Females of species in the Hyh so they are discussed independently.
 Courtship and Matíng
Caecilians her head. The female then nudges the male's cloaca, and 61
The only observaüons of courtship behavior of a caecilian he moves forward, leading the female and fanning her
•ere of captive individuáis of the aquatic typhlonectid with his tail. Upon depositing a spermatophore, he leads
Othonerpeton indistinctum, in which the male coiled her over it, and she pauses with her cloaca over the
about the female and rubbed his body against her prior spermatophore (Briegleb, 1962a). Courtship in Am-
r> copulation (Barrio, 1969). A pair of Typhlonectes phiuma also occurs in water. Unconfirmed observations
aompressicauda observed in copulation were passive for onA tridacíy/um (L Baker, 1937; C. Baker et al., 1947)
about 3 hours; no courtship was observed (Murphy et suggest that courtship may be radically different from that
al. 1977). in other salamanders. Supposedly several females court
a male simultaneously by rubbing him with their snouts
Salamanders from his head backward. Eventually one female enters
The two major trends in salamander courtship are adap- into a mutual embrace with the male, and a spermato-
tations for female persuasión and sperm transfer (Amold, phore is transferred directly to her cloaca. The stream-
1977). Salamanders exhibit many modes of sperm trans- inhabiting Rhyacotriton o/ympicus has a unique tail-wag-
fer and even more differences in behavior that seem to ging display with tail arched forward, just prior to depo-
be tactics for persuasión of females. Salthe (1976) de- sition of a spermatophore (Arnold, 1977).
fcied five stages of courtship in Salamanders: Each of the remaining families of salamanders has
unique courtship behaviors; these families are discussed
1. The male becomes aware of a potential mate, individually.
approaches, and frequently nudges or rubs
the female with his snout. Salamandridae. Courtship usually takes place in water.
2. After ascertaining that the potenüal mate is a Salthe (1967) identified three distinct patterns of court-
female, the male either captures her or blocks ship in salamandrids: (1) caudal capture of the female by
her path and continúes rubbing movements the male and direct transfer of the spermatophore (Eu-
or tail movements. proctus); (2) male capture of female from below and
3. The male moves away from the female; she deposition of the spermatophore on the substrate
follows (not present in all groups). (Chioglossa, Pleurodeles, some Salamandra, Tylototri-
4. The male deposits a spermatophore. ton, and presumably Echinotriton and Salamandrina);
5. The male moves away from the spermato- (3) dorsal capture or no capture of the female and dep-
phore; the female follows him and finds the osition of the spermatophore on the substrate (Cynops,
spermatophore. Notophthalmus, some Salamandra, Taricha, Trituras, and
presumably in the genera Neurergus, Pachytriton, and
These generalitíes are broadly applicable to salaman- Paramesotriton).
ders having internal fertilization, but there are many de- 1. Caudal capture.—Males of Euproctus stand on the
víations from the basic sequence. Hynobiids, cryptobran- tips of their toes with the tail directed laterally. An ap-
chids, and presumably sirenids have external fertilization proaching female E. asper is captured by the male quickly
in water, and there is no known courtship. Males appar- encircling the base of her tail with his tail. Males of £.
entfy take no interest in females until eggs are visibly montanus and E. platycephalus capture females in their
protruding from their vents. However, there may be some jaws and also clasp them with their hind limbs. If the
íorm of male behavior that entices females to males' ter- captured female is quiescent, the male moves into a po-
ritories, for apparently at least in Cryptobranchus alle- sition to place his cloaca near hers and strokes her cloaca
ganiensis (B. Smith, 1907; Bishop, 1941) andHynobius with his feet. Spermatophores are deposited on the fe-
nebu/osus (Thorn, 1963), males select the oviposition male's body, and the male moves the spermatophores
stes. Also, some form of courtship may be present in with his feet to the female's cloaca, after which she is
Ranodon sibiricus, a hynobiid inhabiting mountain streams; released (Bedriaga, 1882).
females apparently deposit egg sacs on top of a prevri- 2. Ventral capture.—Most salamandrids having this
ously laid spermatophore (Bannikov, 1958). pattern court in water, but courtship may begin, or even
Among salamanders with internal fertilization, the pro- be completed, on land in Salamandra. In this genus the
teids court and breed in water. The limited observations male nudges the female's flanks, belly, and throat with
on Necturus indícate that the male swims about the fe- his snout, and in all salamandrids having this pattem, the
male, frequently passing over and under the forepart of male eventually slides under the female and encircles her
her body, which is elevated as she balances on her hind- forelimbs with his from below. In Pleurodeles the prelim-
tirnbs and tail; sperm transfer has not been observed inary rubbing behavior is absent. The male then carnes
(Bishop, 1941). In Proíeus, which lives in subterranean the female around on his back, presumably exposing her
waters, captive males are territorial; courtship consists of to secretions from glands on his dorsum (Salthe, 1967).
the male nudging the female's flanks with his snout and While holding the female, the male deposits a sperma-
working his way anteriorly, eventually blocking her path tophore (Arnold, 1977). Immediately thereafter the male
with his cloaca near her snout and waving his tail about in Salamandra flexes his vertebral column laterally and
LIFE HISTORY
62 the male during a tail-fanning display; (2) duratíon of the
tail-fanning display; and (3) method of partíal capture—
the male placing one forelimb on shoulders of female or
placing a forelimb in front of her snout and a hindlimb
on her back (Kawamura and Sawada, 1959). At this stage
of courtship, the male rubs the glandular side of his head
on the female's snout. Subsequently the male moves
away, followed by the recepüve female, whose attentíon
is focused on his cloaca. Upon deposiüon of a sperma-
tophore, the female passes over the spermatophore, which
adheres to her cloacal lips.
In Taricha and Notophthalmus, there is complete dor-
sal capture of the female; males of both genera have
nuptial excrescences on the inner surfaces of the appro-
priate limbs. In Tarícha, the male clasps the female with
his forelimbs in her axilla and sometímes also pelvically
with his hindlimbs. While holding the female directly be-
low him, the male Tarícha rubs his submandibular gland
on the female's snout, and he may stroke her cloaca with
his hindfeet. Upon dismountíng, he deposits a sperma-
tophore in front of her snout (R. E. Smith, 1941; W.
Davis and Twitty, 1964). In Notophthalmus, after the
male touches the female's cloaca with his snout, he clasps
Figure 3-18. Capture positions in salamandrids (males shaded). her from above and works his way forward until his hind-
A. Notophthalmus viridescens embracing female and rubbing her
snout with his genial glands. B. Tarícha torosa embracing female limbs encircle her axilla or neck (Fig. 3-18). After capture,
and rubbing her snout with his submandibular gland. Adapted from the male arches his body laterally and rubs the side of
Arnold (1977). his head (genial glands) on the snout of the female and
simultaneously fans the side of her body with his tail.
pivots approximately 45° on the contralateral forelimb; Subsequently the male dismounts and leads the female,
this lateral displacement of the posterior part of his body who nudges his cloaca with her snout; presumably this
allows the female's cloaca to drop onto the spermato- nudging triggcrs spermatophore deposiüon (A. Hum-
phore (Hafeli, 1971; Joly, 1966). In Pleurodeles the male phries, 1955).
deposits a spermatophore and pivots 180° to face the The European newts, Triturus, are unique in that the
female, who drops on the spermatophore (Arnold, 1977). male does not grasp the female during courtship. The
3. Dorsal capture or no capture.—There is consid- extensivo fins and bright color pattems of the breeding
erable diversity in behavior in salamandrids having dorsal males provide visual stimuli to the females. Extensive
capture or no capture at all. Only in this group is there investigations of courtship behavior of European newts
direct evidence of chemosensory sex and species iden- by Halliday and coworkers (summarized in Halliday, 1977)
tificatíon. Twitty's (1955,1961) experiments with Tarícha have demonstrated the primary significance of visual sig-
are especially illuminating. Male T. rivularis were at- náis and stereotyped sequences of behavior by both sexes.
tracted to sponges soaked with skin secretions from con- Females play an important role in the timing of successive
specific females, but ignored sponges that lacked secre- sequences, because the male is dependent on feedback
üons. Females of four populaüons of Tarícha (rívularis, from her. Furthermore, this timing is important in the
granulosa, torosa torosa, and torosa sierrae) were an- completion of the courtship sequences, for if the female
chored side by side in a stream naturally inhabited by T. is not sufficiently responsive, the male must interrupt
rivularis and T. granulosa. Natíve male T. rivularis showed courtship and swim to the surface for breathing.
a strong attraction to conspecific females and females of As an example of the complex courtship behavior in
T. torosa sierrae but a weak response to others. Blinded European newts, the following description of courtship in
males of T. rivularis were able to disünguish conspecific Triturus vulgarís is summarized from Halliday (1977) (Fig.
females. Females of Triturus cristatus can distinguish se- 3-19). The male usually initiates sexual encounters. He
cretíons of males from those of females (Cedrini and Fa- walks or swims around in a pond; when he meets a
solo, 1971). female he sniffs at her cloaca and attempts to position
In Cynops pyrrhogaster, the male nudges the female himself in front of her. Usually the female moves away;
with his snout, beginning at her cloaca and proceeding she is pursued by the male, who again attempts to place
to her head; he then blocks her path with his head. From himself in front of her. The sequences of this orientatíon
this point in the courtship, patterns vary in different geo- phase are repeated several times. Once the female stops
graphic races. These variations include: (1) position of moving, the male remains in front of her and initiates a
 Courtship and Mating
63

Whip

Spermatophore Deposition
and
Quiver Transfer

Creep-On and
Follow

Touch Tail Deposition

Ftgore 3-19. Courtship of European newt Trituras vulgaris (male shaded). Spatial movements indicated by
soHd arrows; other sequences are stationary. Open arrow indicates position of spermatophore. Redrawn from
Halliday (1977).
LIFE HISTORY
64 ward the female and resumes his retreat display; the fe-
male approaches again. During a sexual encounter, the
courtship sequence is usually performed two or three
times. Apparently there is no signal from the female to
the male when she picks up the spermatophore, for he
is just as likely to proceed with another courtship se-
quence after a successful bout as he is after an unsuc-
cessful one.

Ambystomatidae. A review of courtship patterns in

Ambystoma by Salthe (1967) and detailed studies on A.
macu/atum and A. íigrinum by Amold (1976) reveal some
basic pattems and specific variatíons. With the exception
of A. opacum, courtship takes place in water. Most spe-
cies have rather short breeding seasons; males arrive at
ponds first and are followed by females. Dorsal capture
of females by males is known in only four species. In
three of these (jeffersonianum, laterale, and macrodac-
Figure 3-20. Tail-nudging walk in Ambystoma mexícanum, tylum), the males clasp the females anteriorly with their
showing female nudging male's cloacal papillae while male
(shaded) moves forward and waves tail laterally. Redrawn from forelimbs, but in A. graci/e the clasping is also with the
Arnold (1977). hindlimbs around the female's axilla. In these species
(except A. graci/e,) the male rubs the female's snout with
his chin. Subsequently the female is released and the
display of tail movements—wave, whip, and fan. These male leads her, and he deposits a spermatophore on the
displays are not only visual but also tactile (water cur- substrate.
rents) and olfactory. The wave consists of the male hold- In the other species of Ambystoma that have been
ing his tail up for about 1 second, thereby giving the studied, the male nudges and rubs an uncaptured female
female a full lateral view of his body and tail. The whip and leads her to a spermatophore, deposited immedi-
is a sudden, forceful movement, in which the tail, from ately in front of her snout or (as in A. macu/atumj some
the wave posiüon, is lashed against the male's flank, distance away; in the latter case the male retums to the
creating a water current of sufficient power that it may female and leads her to the spermatophore. In most spe-
push the female backward. The fanning movement is cies the female follows the male with her snout cióse to
relaüvely weak and sustained for periods up to half a his cloaca, and spermatophore depositíon may be trig-
minute; the tail is curved against the flank nearest the gered by her prodding his cloaca with her snout (Fig. 3-
female, and its distal portion is vibrated at a rate of about 20). In A. tigrínum the male forcefully pushes the female
six beats per second, generating water currents directed through the water and then initiates a tail-nudging walk.
toward the female's snout. The wave provides a visual In A. mexícanum, opacum, and talpoideum, the male
signal, and the whip is primarily tactile, whereas the fan- also focuses on the female's cloaca, sometimes resulting
ning movements are thought to transmit odors from the in a snout-to-vent circular sequence before the male leads
male to the female. Bouts of stationary display are con- the female forward prior to deposition of a spermato-
tínued until the female approaches the male, who then phore. Males usually deposit several spermatophores and
retreats before her while maintaining his orientaüon and repeat courtship sequences several times.
display—mostly whips with very few waves or fans. The As a detailed example of Ambystoma courtship, the
retreat lasts 5-60 seconds, at which time the male ceases following account of courtship in A. talpoideum is sum-
to display, turns, and moves away from the female; she marized from Shoop (1960) (Fig. 3-21). All activities take
follows him. He creeps for a distance of 5-10 cm, stops, place in shallow water, with the salamanders moving about
and slowly quivers his tail with her snout; the male folds on the bottom. Courtship is initiated by the male nudging
and raises his tail and deposits a spermatophore on the the head of the female with his snout for about 10 sec-
substrate. Immediately the male creeps away and turns onds; then he moves his snout posterior to her cloaca,
perpendicularly with his tail folded against his flank near- at which time the female puts her snout in the male's
est the female. She moves forward and presses against cloacal región. Both push with their heads, which results
his tail, which serves to brake her progress. The male in a circular movement. After one or two revolutions, the
resists her pressure and may flex his body and tail so as male straightens his body, and the female slides her snout
to push her back. These maneuvers result in the female to the tip of his tail. At this point, the male initiates a
being positioned with her cloaca above the spermato- lateral shuffling of his pelvic región and fans the posterior
phore, which becomes attached to the cloaca. From the part of his tail, which frequently touches the female's
braking position or after pushbacks, the male tums to- head. Using only the forelimbs for propulsión, the male
 Courtship and Matíng
65
2. Nudge S.Waltz
1. Approach
8. Male and Female Sepárate
(¡f spermatophore picked up)
V
I
7. Spermatophore
Pick-up
5. Cloacal Bump
and
Spermatophore
6. Nose Spermatophore Deposition
Figure 3-21. Courtship in Ambystoma talpoídeum (male shaded). Spatial movements indicated by solid
arrows; other sequences are stationary. Open arrow indicates position of spermatophore. Adapted from
Shoop (1960).
LIFE HISTORY
66 the female being abraded by the teeth of the male and
the mental gland secretions being introduced directly into
the female's superficial circulation. Other plethodontids,
such as Eurycea bislineata, Aneides lugubris, and Hydro-
mantes platycephalus, pulí their chins in a succession of
quick strokes on the dorsum of the female. Large species
of Plethodon (glutinosas, jordani, and yonahlossee) de-
liver mental gland secretions by slapping the gland on
the female's snout (Fig. 3-23). Species that lack mental
Figure 3-22. Inoculation of témale by male Eurycea bísllneata in glands and elongate premaxillary teeth (e.g., Pseudotri-
water. Male (shaded) pulís mental gland and premaxillary teeth
along dorsuin of témale. Redrawn from Arnold (1977). ton ruber, Ensatina eschscholtzi) have not been observed
to perform any of these kinds of actions.
As an example of plethodontid courtship behavior, the
following description of the behavior of Plethodon jor-
dani has been summarized from the extensive work of
Arnold (1976) (Fig. 3-24). Courtship takes place on land.
Upon contacting a female, the male moves along the side
of her body while tapping her dorsum with his head,
nudging her flanks with his snout, or sliding his chin an-
teriorly along her back. The male also may perform a
"foot dance"—raising and lowering either forelimbs or
hindlimbs one at a time. During these sequences, the
male apparently identifies the sex and species by che-
Figure 3-23. Snout-slapping of témale by male (shaded) moreception. Upon identifying a conspecific female, the
Plethodon jordani, as a means of applying secretions from mental maleJocates her head and attempts to initiate the tail-
gland, during the tail-straddling walk while the male undulates the
base of his tail. Numbered arrows indícate sequence and direction straddling walk by nudging or sliding his mental gland
of movements. Redrawn from Arnold (1977). along her cheek or snout and placing his head beneath
her chin and lifting her head. He then crawls forward
moves slowly forward while continuing the lateral shuf- under her chin. When the female's chin comes in contact
fling and tail-fanning. The female follows, keeping her with the dorsal base of his tail, he arches the base of his
head in contact, or nearly so, with the male's tail. After tail and undulates it laterally and begins walking. If the
she follows him for 1-11 minutes, the female moves for- female does not maintain contact with the base of the
ward and nudges the male's cloacal región one or two male's tail, he stops undulating his tail and after a few
times. He then terminales pelvic and caudal movements, minutes turns around and initiates courtship again. The
deposits a spermatophore, resumes the movements, and tail-straddling walk continúes for several minutes to more
slowly moves forward. The female noses the spermato- than an hour; during this time the male apparently relies
phore and crawls over it. Meanwhile the male continúes solely on tactile cues to monitor and regúlate the female's
slow forward motion, pelvic shuffling, and tail-fanning. If position. While in the tail-straddling walk, the male may
the female picks up the spermatophore, she terminales turn periodically and slap his chin (mental gland) on the
her association with the male; if she does not pick up the female's snout. Once the female sudes her chin anteriorly
spermatophore, she continúes following the male with along the base of the male's tail, he lowers his vent and
her head in cióse association with his tail. slides it along the substrate. This vent-sliding lasts for no
more than 1 minute and presumably represents a tactile
Plethodontidae. All plethodontids, whether courting search for a suitable site for deposition of a spermato-
on land or in water, engage in a tail-straddling walk—a phore. Upon depositing the spermatophore, the male
behavior unique to this family (Arnold, 1977). Males of moves forward and flexes his tail laterally from beneath
most plethodontids have well-developed mental glands, the female; he continúes forward with the female's chin
and many have protruding premaxillary teeth. The ap- still resting on the base of his tail. He stops when the
plication of mental gland secretions to the female occurs spermatophore is in contact with her vent; she makes
in those species having the glands. The method of ap- slight lateral movements with the base of her tail, lowers
plication of the gland to the female is variable. In some her vent onto the spermatophore, and picks it up in her
plethodontids, the application is by "vaccination" of the cloaca.
female with the premaxillary teeth (Fig. 3-22). In Des-
mognathus, some small species of Plethodon, and some
bolitoglossines, the male presses the gland against the
Anurans
female's dorsum and then flings himself away with a Identification of Mates. The major factor in anuran
snapping motion. This motion results in the surface of courtship is the production of advertisement calis by males;
 Courtship and Maüng
67
2. Initiation of Tail-Straddling Walk
1. Approach and
Cheek-Rub
3A
3. Tail-Straddling
Walk
4. Spermatophore
De position
and
Transfer
Figure 3-24. Courtship of Plethodon jordani (male shaded). Spatial movements are indicated by large solid
arrows; small solid arrows indícate tail movements. Open arrow indicates position of spermatophore.
Adapted from Arnold (1976).
LIFE HISTORY
the complexity of vocalizatíon and associated behavior is ature and heavy rainfall initiate migrations to breeding
treated in detail in Chapter 4. Compared to salamanders, sites—frequently temporary ponds. Explosive breeders
olfactory cues and visual displays seem to be unimportant include Scaphiopus and many species of Bu/o, Gastro-
in preamplectic courtship in most anurans, but some tac- phryne, and Rana sylvatica in North America; many spe-
tile cues are used by certain species. The diversity of cies of Cyclorana, Litaría, Limnodynastes, and Neoba-
glands developed by various male frogs in the breeding trachus in Australia; Pleurodema brachyops and many
season suggests that olfactory cues may be used at least species of Leptodactylus, Physalaemus, Bufo, Hyla, and
in sex recogniüon. This might be especially important in O/o/ygon in the llanos in northern South America; and
species that breed in water. G. Rabb and M. Rabb (1963a) Pyxicephalus adspersus and various species of Bu/o and
suggested that secretions from the postaxillary glands in Hyperolius in South África. In most of these species, fe-
Hymenochirus boettgerí may repel other males or attract males are attracted to the breeding site by male vocali-
females; furthermore, because the glands are distinctly zations. In high densities, males usually search actively
colored, it is possible that visual identification is made. for females at the breeding site and apparently cannot
The absence of sexual color differences in most anu- discrimínate visually between the sexes. However, males
rans suggests that visual cues may be unimportant in of some species remain in a restricted área and attempt
identificación of potential mates, at least in nocturnal spe- to amplex only those frogs that approach closely; this
cies. Experiments on species and sex identification in Hyla limited-area searching is known in some species of Bom-
cinérea and H. gratiosa provided no evidence for visual bína, Discog/ossus, Pelobates, Scaphiopus, Bufo, and Rana
cues in these nocturnally breeding species (H. Gerhardt, (see Wells, 1977b).
1974b). On the other hand, Bufo canoras and B. peri- Among species having prolonged breeding seasons,
glenes breed by day and have striking sexual color di- females usually approach individual males and usually
morphism. Male ranids, Staurois parvus, apparently at- the male continúes to cali until touched by the female.
tract females by visual display; males on boulders in streams Female Hyla rosenbergi enter, inspect, and even modify
slowly and deliberately extend a leg and spread the toes, the nest in which a male is calling before she positions
thereby exposing palé blue webbing, which contrasts with herself for amplexus (Kluge, 1981). Physical contact of
the otherwise cryptic coloration (Harding, 1982). With the male by the female is not universal. For example,
the exception of black throats in males, there are no female Hyla ebraccata move to within 6-30 cm of a
pattern differences among the sexes of most dendroba- calling male and orient the flanks to the male, who ter-
tids, all of which breed by day. Visual cues to potential minates calling, tilts his head in the direction of the fe-
mates, as well as to male adversaries, may be enhanced male, and jumps to her, positioning himself adjacent and
by the posture of breeding males; usually they hold their parallel to the female before initiating amplexus (Miya-
heads high, thereby making the throat more visible. moto and Cañe, 1980a). Pairs of Agalychnis callidryas
Tactile cues probably are the most important nonvocal have been observed nearly face to face on a limb; then
factors in mate identification in anurans. Differences in the female turns 180° and the male mounts her (Pybum,
size and skin texture have been shown to be used in sex 1970). Female Polypedates leucomystax have been ob-
identification. Amplexus is stímulated by the greater girth served to sit perpendicular^ in front of a calling male,
and firmness of the female in such diverse frogs as Rana who turns 90° and mounts the female from the side (C.
selvática, Hyla andersonii, Ascaphus truei, ana Pipa pipa. Johnson and Lowery, 1968).
However, in Bufo, males and spent females usually give Some distinctive preamplectic and amplectic behaviors
reléase calis when clasped by a male. Size differences are known, especially among pipid and dendrobatid frogs
may be especially important in species recogniüon among (treated later in the section: Other Courtship Behaviors).
sympatric and synchronously breeding congeners. Thus, In the terrestrial-breeding Synhophus marnocki, the fe-
males of B. americanus discrimínate against females of male moves about the male, who scratches her dorsum
the larger B. woodhousii in favor of the smaller conspe- with his hindfeet; when she stops moving, he mounts her
cific females (A. Blair, 1942). Males of Gastrophryne car- in amplexus (Jameson, 1955a). Upon the initiation of
olinensis discrimínate against the smaller females of G. amplexus, the male of the pouch-brooding hylid F/ec-
olivaceus (A. Blair, 1950). Sexual differences in skin tex- tonotus pygmaeus kicks the back of the female and in-
ture presumably are effective means of sex identification serts his feet into the pouch (Duellman and Maness, 1980).
among many species of toads, especially those that do
not vocalize, such as members of the Bu/o spinu/osus Amplexus. When both the male and the female are
group. ready to mate, the male usually grasps the female so that
Tactile identification probably is most important in those he is dorsal to her. This embrace, amplexus, is inguinal
species that are explosivo breeders, that is, species that in the primitive frogs, including all archaeobatrachians,
congrégate in large numbers for intense breeding activity myobatrachids, and some telmatobiine leptodactylids
for a short period of time (Wells, 1977b). Short-term, (J. D. Lynch, 1973), and sooglossids (Nussbaum, 1980).
dense breeding aggregations are especially prevalent in With the male's forelimbs grasping the female around the
highly seasonal regions, where combinations of temper- waist, the vents are not juxtaposed; presumably this
 Courtship and Mating
69

! 3-25. Amplectic positions in anurans (males shaded). A. Inguinal (Alytes obstetricans). B. Axillary
VEJeutherodactylus danae). C. Cephalic (Colosthetus inguinalis). D. Straddle (Mantidacfylus líber). E. Glued
Breviceps adspersus). f. Independent (Dendrobates granuliferus). Drawing C adapted from Wells (1980a); D
adapted from Blommers-Schlosser (1975a), and E adapted from Wager (1965).

method of amplexus is not as efficient for ensuring fer- remain attached for 3 days. Although they may maintain
tfflzation of eggs as is the more forward position, axillary a weak axillary amplexus, some other heavy-bodied mi-
amplexus, which places the vents closer together (G. Rabb, crohylids also are adherent during amplexus; this is known
1973). Most neobatrachians have axillary amplexus. in the Philippine Ka/ou/a con/uncía and K. picta (Inger,
However, there are some notable exceptíons in both 1954) and the North American Gastrophryne carolinen-
groups (Fig. 3-25). Amplexus initially is inguinal in the sis (Conaway and Metter, 1967) and G. olivácea (Fitch,
European midwife toad, Alytes obstetricans, bul as the 1956). Specialized secretory cells in the dermis of the
eggs emerge, the male shifts to a cephalic embrace and venter of the male provide the adhesive substance in G.
draws his legs up through the eggs, which adhiere to his caro/inens/s (Conaway and Metter, 1967) and presum-
legs (Crespo, 1979). Inguinal amplexus is a secondary ably in the other microhylids exhibitíng this behavior.
adaptive conditíon in some neobatrachians. In the small, A unique, ventral inguinal amplexus occurs in two spe-
fossorial microhylid Myersiella microps, the male in in- cies of bufonids, Nectophrynoides malcolmi and N. oc-
guinal amplexus does not créate a larger overall diameter cidentalis, in which fertilization is internal. Some other
for the pair than that of the female, which burrows head species of Nectophrynoides, two of which are known to
first through mulch (Izecksohn et al., 1971). The same have internal fertilization and one with external fertiliza-
might be true for the African terrestrial hyperoliid Chry- tion, have normal, dorsal amplexus (Grandison, 1978).
sobatrachus cupreonitens, in which the comparatívely small Axillary amplexus normally involves the male grasping
male has short forelimbs (Laurent, 1964). the female in the axilla; in those species having nuptial
In some anurans with globular bodies and short limbs, excrescences, the pads or spines are pressed tightly into
effecüve axillary amplexus is not possible. Thus, the small the axilla. In many tree frogs (Phyllomedusa, Litoria, Chi-
Andean toads, Osomophryne exhibit inguinal amplexus romantis), one or two fingers are placed above the arm
(Ruiz and Hernández, 1976). Males of the African mi- of the female. In all cases the palms are medial. In the
crohylids of the genus Breviceps are glued to the pos- nest-building frog Hyla rosenbergi, the female is grasped
terior part of the dorsum of the female (Wager, 1965); by the angle of the jaw (Kluge, 1981); the sexes in this
in this position they both dig with their hindfeet and may species are nearly the same size, so a more forward po-
LIFE HISTORY
sition of the male resulte in the venís being closer to- Other Courtship Behaviors. Elabórate and diverse
gether. courtehip behaviors are known in the diurnal, terrestrial
Some dendrobatids have cephalic amplexus, in which dendrobatid frogs. The differences in courtehip activities
the dorsal surfaces of the male's hands are pressed against of these frogs, as compared with those of most other
the female's throat; this form of amplexus is known in anurans, seem to be associated with aggressive defense
Cohstethus inguinalis (Wells, 1980a), Dendrobates tri- of territories by either males or females and the absence
color, Phyllobates aurotaenia, and P. tembilis (Myers et of amplexus in many species. In anurans in which the
al., 1978). Amplexus is absent in Dendrobates granuli- pair is in amplexus prior to oviposition, the female usually
ferus, D. pumilio, and Rhinoderma (Crump, 1972; Lim- chooses the oviposition site (oviposition in nests con-
erick, 1980; Pflaumer, 1936). In some Madagascaran structed by the male prior to mating, as in the Hyla boans
ranids—Mantidactylus blommersae, depressiceps, and líber group, is an obvious exception). However, in dendro-
—the male sits astride the head and shoulders of the batids the male usually selects the oviposition site. The
female on a vertical leaf during rain; presumably sperm complex courtship behavior in dendrobatids was sum-
flow down the female's back to ferülize the eggs depos- marized by Wells (1977b, 1980a, 1980b) and H. Zim-
ited on the leaf (Blommers-Schlósser, 1975a; 1979a). mermann and E. Zimmermann (1981). Males of all spe-
Some terrestrial Madagascaran ranids have abbreviated cies are highly vocal. In some species that do not exhibit
amplexus; Mantella aurantiaca has a short, loóse am- aggressive defense of territories, additional behavior in-
plexus, after which eggs are deposited amidst leaves (Ar- volves tactile courtship of the male by the female (Table
noult, 1966), and similar abbreviated amplexus occurs in 3-1). For example, in Dendrobates auratus the female
Mantidactylus curtas, which has aquatíc eggs (Amoult jumps on the male's back and prods him with her fore-
and Razariheliosa, 1967). Discoglossus, which deposite limbs. In those species in which the males aggressively
aquatíc eggs, also are in amplexus for only a few seconds defend territories, females approach males, but in species
(Knoepffler, 1962). of Cohstethus in which females aggressively defend ter-
Superimposed on the general pattern of inguinal am- ritories, males approach females. Tactile courtehip of fe-
plexus in primitíve frogs and axillary amplexus in ad- males by males includes prodding, jumping on the back
vanced anurans are a variety of modifications relatíng to of the female, or an abbreviated cephalic amplexus. Vis-
relatíve body size and shape of the sexes, parental care, ual displays by males include jumping up and down in
and mode of oviposition. The abbreviated amplexus be- front of the female, a "toe dance" in C. collaris, and
fore, but not during, oviposition in some frogs may pro- notable darkening of color in C. palmatus, trinitatus, and
vide the sümulation for ovulation, but is unnecessary to possibly collaris.
ensure fertilization. Courtehip and mating in pipids takes place in water.
In most anurans, amplexus occurs at or near the ovi- These behaviors have been described in detail for Hy-
position site, and pairs remain in amplexus for only an menochirus boettgeri (G. Rabb and M. Rabb, 1963a),
hour or two. The duration of preovipositional amplexus Pipa pipa (G. Rabb and M. Rabb, 1961, 1963b), and P.
probably is related to the time required for the female to carvalhoi (Weygoldt, 1976a). In Hymenochirus boettgeri,
find a suitable oviposition site. However, once in am- calling males shuffle their feet and move their arms in a
plexus, female Hyh rosenbergi inspect and modify the manner similar to clasping; they respond to movemente
nest prior to laying eggs (Kluge, 1981). Pairing of Brev- of other frogs and usually approach potential mates from
iceps adspersus takes place on the surface of the ground; the flank. An attempt to clasp a male usually resulte in
subsequently the pair (male adhered to the posterior part immediate reléase in response to an abrupt, vibratory
of the female) dig a nest chamber. Pairs have been ob- buzz given by the other male. When clasped by a male,
served adhered together for 3 days prior to oviposition unreceptive females assume a tonic posture with the legs
(Wager, 1965). Pairing in the Andean bufonid Atelopus outetretched; if the male does not reléase her, the un-
oxyrhynchus takes place on the forest floor; subsequently receptive female may twitch her arms, wave her feet,
the amplectant pair moves to a stream for egg-laying. quiver her entire body, or lunge under an object in an
One pair was in amplexus for 125 days (Dole and Dur- apparent attempt to dislodge the male. Rejection actions
ant, 1974a). A pair of A. varius was observed in am- by a female may be inhibited by the male pumping his
plexus for 20 days (P. Starrett, 1967). Similar long-term arms. The stimulus for oviposition presumably is pro-
amplexus occurs in A. ignescens; pairs transported from vided by the male stroking the female's head with his
the field to the laboratory remained in amplexus for more feet. Similar courtehip activity occurs in Pipa pipa and
than a month. Pernales of the desert-dwelling myoba- carvalhoi. The tonic posture of an unreceptive female
trachids Arenophryne rotunda and Myobatrachus gouldii also occurs in Ascaphus truei, which mates in water (No-
approach calling males on the surface of the ground and ble and P. Putnam, 1931).
then burrow deep into the ground (up to 1 m) where the Courtehip behavior during amplexus has been re-
pair remains together for 5 or 6 months before depositing ported in few anurans. In addition to the pipids, arm
eggs, which undergo direct development (Roberts, 1981, pumping and up and down movemente of the head of
1984). the male occur in Pelobates fuscus, the male of which
 Courtship and Mating
TaMc 3-1. Courtship in Dendrobatíd Frogs, Genera Dendrobates and Colostethusf 71
Territorial Tends Cantes Approaches Selecta
Species defense eggs tadpoles mate site Courtship activity
D. ouratus
—
3 <J 9 <J Tacüle courtship of 3 by 9
O. ozureus — 3 3b 9 ? Tactíle courtship of 3 by 9
D. granu/i/erus 3 ? 9 9 3 Tactíle courtship of 9 by 3
D. pumi/io 3 í 9 9 3 Visual and acoustíc courtship of 9 by 3 ;
temporary cephalic amplexus
D. te/imanni 5 9 9 9 9 3 pursues 9 ; tactile courtship by both
D. histrionicus d 9 9 9 9 3 pursues 9 ; tactile courtship by both
C inguina/is íc ? 9 9 3 Tactile and acoustic courtship by 3 ;
cephalic amplexus
C pa/matus <?, 9 c? 3 9 3 Tactile and acoustic courtship by 3
C íriniíatus 9 c? 3 3 3 Acoustic and visual courtship by $
C. co//aris 5 7 3 ?3 3 Acoustic and visual courtship by 3
TtoSáy summarized from Wells (1977b) and H. Zimmermann and E. Zimmermann (1981). Témales defend temporary territories.
"ftbo sometímes by females.

aiso scratches the female's cloaca with his hindfeet while

in amplexus (Eibl-Eibesfeldt, 1956). Male Bambino var-
iegata aiso pump their arms and quiver the entíre body
«¿ule amplecting a female (R. Savage, 1932). While in
amplexus, the male Bufo mazatianensís undergoes con-
vulsive shudderings and thumps his outer toes against
the female's feet (Firschein, 1951). These diverse obser-
vations provide no insights into the significance of these
actions. Apparently these movements on the part of the
male provide some kinds of signáis or stimuli to the fe-
male; in some instances such actions presumably induce
ovulation by the female.

FERTILIZATION AND OVIPOSITION

Fertilization occurs externally at the time of oviposition in
most anurans and in primitive salamanders, whereas fer-
tíüzation is interna! in caecilians, most salamanders, and
a few anurans. In amphibians having internal ferülization,
oviposition may occur from a few hours to many months
after mating.

External Fertilization
Figure 3-26. Ovipositional sequence in Pseudacris tríseríata (male
Salamanders. Primitive salamanders deposit eggs in shaded). A. Shielding posture of male as female rests, grasping
water—strings of eggs in cryptobranchids and a pair of stem in water. B. Concave arching of back of female.
C. Downward thrust of male as oviposition begins. D. Adherence
egg sacs in hynobiids. The male moves over the eggs of eggs to stem. Modified from Gosner and Rossman (1959).
and releases sperm. The male of Hynobius nebulosus
grasps the egg sac in fore- and hindfeet and crawls along
the sac and rubs his cloaca over it (Thorn, 1963). The evidence for various kinds of tactile signáis between the
stream-dwelling hynobiid Ranodon sibiricus has a sper- sexes. Once the female has selected an oviposition site,
matophore but retains external ferülization. The male de- peristaltic abdominal contractions in the female accom-
posits a spermatophore, and the female places eggs on pany ovulation or movement of eggs down the oviducts
top of it (Bannikov, 1958). During oviposition, the male and may signal the male that oviposition is about to take
and female salamanders are not in contact; if any stimuli place. Oviposition and fertilization are accomplished by
influence the timing of oviposition, they must be olfactory synchronized movements by both partners. A male in an
or visual. inguinal embrace may be able to detect abdominal
movements by the female, including muscular activity of
Anurans. At the time of oviposition and fertilization in the oviduct. However, a male in axillary amplexus may
most anurans, the pair is in amplexus, and there is some not be aware of oviducal contractions.
LIFE HISTORY
** Among anurans with inguinal amplexus, the male usu- juxtapositíon with hers, and ejaculates as eggs are de-
ally arches his back, bringing his cloaca adjacent to that posited (Fig. 3-26). This pattern is essentially the same
of the female, and ejaculates as she releases eggs. This in all anurans having axillary amplexus and depositing
behavior is modified in Alytes obstetricans, for during their eggs in water. In some species, such as most species
ovipositíon the male shifts forward on the body of the of Rana that deposit their eggs in a single clutch (Fig. 3-
female. 27), there are one or more massive extrusions of eggs,
1. Aquatíc ovipositíon.—Among anurans with axil- while the pair remains essentially statíonary in the water.
lary amplexus, the abdominal contractíons of the female Litaría splendida forcefully expels eggs through a sperm
and posiüoning of the hindlimbs presumably are signáis suspensión in quiet water (M. J. Tyler, pers. comm.); a
to the male that the female is ready to oviposit. Usually similar manner of ovipositíon occurs in Hyla andersonii
the female arches her back ventrally and raises her cloaca; (Noble and Noble, 1923). Males of L. verreawá cup their
the male arches his back dorsally, brings his cloaca into feet around batches of eggs as they are extruded and

Figure 3-27. Egg clutches of Rana

píplens in shallow water at Iris
Springs, Arizona. Photo by J. S.
Frost.

Figure 3-28. Egg strings of Bufo

americanas in shallow water at
Myersville, Maryland. Photo by K.
Nemuras.
 Courtship and Mating
faold the eggs momentarily adjacent to their venís before and inner surfaces of the thighs of the male; the eggs 73
pushing them to the feet of the female, which holds them spread out in a surface film (B. Balinsky and J. Balinsky,
far nearly 1 minute before she begins climbing around a 1954). While ovipositing, female Phrynohyas venulosa
spbmerged twig and wrapping the eggs around it with víbrate the vent laterally (Pybum, 1967); this acüon seems
her feet; similar oviposition behavior occurs in Litaría to spread the eggs out on the surface of the water.
tirapo, dentata, and glauerü (Anstis, 1976). Female Bu/o In some pipids complex oviposition maneuvers take
osually walk around in shallow water while ovipositing, place in water. There seems to be an evolutionary trend
so that the eggs are distributed as a pair of strings (one from ordinary midwater deposition of eggs on plants (some
fcom each oviduct) (Fig. 3-28). Small strands of about Xenopus), to upside-down oviposition on plants (some
20 eggs are ejected during successive depositions by Ma- Xenopus), to egg-laying turnovers at the surface of the
aogenioglottis a/ipioi; the male kicks the eggs, dispersing water (Hymenochirus and Pseudhymenochirus), to mid-
ten in the water (Abravaya and Jackson, 1978). In those water turnovers with the adhesión of eggs on the dorsum
spedes that deposit their eggs as a film on the surface of of the female (Pipa) (G. Rabb, 1973). During the ovi-
fie water (Fig. 2-12), the female usually is below the position sequence in Hymenochirus boettgeri (Fig. 3-29),
surface with only her vent out of water. During oviposi- the pair swims to the surface; the frogs may or may not
fon. the female Pyxícephalus adspersus moves up and take in air, then turn over, thrust their venís above the
down and sideways, rubbing her vent against the belly surface and expel eggs and sperm, and turn over again

(•re 3-29. Ovipositional maneuvers in Hymenochirus boettgeri (male shaded). A. Resting on bottom.
Ascent. C. Breathing. D. Turnover and oviposition on surface. E. Turnover and descent. In sequences in
frogs breathe (C), they usually sink slightly below the surface before turning over (D). Horizontal line
surface. Adapted from G. Rabb (1973).
LIFE HISTORY
• ** on their way to the bottom. The female leads the male occur in Pipa pipa (G. Rabb and M. Rabb, 1961,1963b)
through these maneuvers. While the pair is upside down and P. carvalhoi (Weygoldt, 1976a), but the eggs are
at the surface of the water, the male kneads the female's deposited on the dorsum of the female during midwater
abdomen, and both individuáis flex their legs and move turnovers and rotations (Fig. 3-30). During each turn-
their feet forward and backward, presumably to maintain over, a few eggs are extruded and are caught against the
balance. As the eggs are expelled, they pass posteriorly belly of the male, which then makes forward thrusts with
toward the male's vent, which is simultaneously brought his vent región, presumably fertílizing the eggs; as the
forward toward the eggs. The oviposition sequence is pair settles to the bottom, the male presses the eggs to
repeated untíl all eggs are laid. If the female slows her the female's dorsum, where they adhere and implant.
turnover movements, the male may initiate arm pumping 2. Arbórea/ ovipositíon.—Egg-laying on leaves or
and foot stroking. Four matíngs included 51, 143, 154, branches of bushes or trees is accomplished in much the
and 346 turnover sequences resulting in 20, 400, 500, same way as aquatic oviposition, except that the male
and 1047 eggs, respectively (G. Rabb and M. Rabb, maintains cióse contact with the dorsum of the female,
1963a). Usually no eggs are expelled during the first turn- and their vents are continuously juxtaposed. Two kinds
over and several of the last turnovers. The duration of of ovipositional behav/ior have been observed in phyl-
each oviposition sequence is about 6 seconds, and the lomedusine hylids (Kenny, 1966; Duellman, 1970; Py-
enüre oviposition process requires 1.5-7 hours. burn, 1970, 1980a). In Aga/ychnis ca//idryas and Pachy-
Similar courtship activity and oviposition maneuvers medusa dacnicolor, the female (with the clasping male

Figure 3-30. Ovipositional maneuvers in Pipa carvalhoi (male shaded). A. Midwater swimming. B. Rest on
bottom and push off. C. Ascent and turnover. D. Turnover and capture of eggs against belly of male. E. Sink
to bottom and placement of eggs on dorsum of female. Horizontal line is water surface. Adapted from
Weygoldt (1976a).
 Courtship and Mating
75

: 3-31. Oviposition by Phyllomedusa hypocondríalis at Figure 3-32. Egg clutches of Phyllomedusa duellmani,
Bdém, Brazil. Eggs can be seen just to the right of the male's right Departamento Amazonas, Perú. Leaf to the left has been opened to
leg. Note the grasping of the edge of the leaf by the hindfeet of the show eggs and eggless capsules, whereas leaf to the right is folded
e. Photo by W. E. Duellman. and adherent to eggs as completed by the amplectant pair. Photo
by D. C. Cannatella.

on her back) desceñas to the pond where she takes water depressions or burrows, or in trees is widespread in sev-
into her bladder; she then climbs up into overhanging eral groups of primarily tropical anurans (see Chapter 2).
vegetation and deposits a clutch of eggs, releasing water In leptodactylids, the male constructs the nest with his
from her bladder over the eggs as they are laid. Subse- hindfeet while in amplexus. The actual construction of
quent clutches are deposited by the same pair but only the nest differs in various species. Males of Leptodactylus
after they descend to the water again. Female Phyllo- pentadactylus move both feet simultaneously in lateral
medusa do not descend to water prior to oviposition, and motions, stirring the water and air with the eggs, jelly,
some species are known to fold the leaf over the eggs as and sperm as they are emitted (Heyer and Rand, 1977).
they are being deposited on it. Typically, an amplectant In Physalaemus pustulosus, the male kicks his legs alter-
pair deposits eggs on the upper surface of a leaf and nately into the mixture (Fig. 3-33). As the female Pleu-
moves forward (upward) on the leaf as oviposition con- rodema brachyops releases eggs, the male holds small
tinúes; the margin of the leaf is grasped by the feet of quantities of spawn with his hindlegs at the surface of the
both members of the pair (Fig. 3-31). Upon completion water and then beats the eggs into a foam by rapid criss-
of oviposition the leaf is entírely wrapped around the egg cross motions of the feet (Hoogmoed and Gorzula, 1979).
clutch; eggless capsules are deposited during the ovipo- Large quantities of seminal fluid are released by males
sition, and these capsules provide moisture for the de- of species that have terrestrial foam nests; in Leptodac-
veloping eggs (Fig. 3-32). Similar nests are constructed tylus bufonius, the male vigorously whips the seminal
by hyperolüds of the genus Afrixalus, some of which do fluid, jelly, and-eggs into a foam with his hindfeet (Pisano
so under water (Wager, 1965). and del Río, 1968).
3. Foam-nest construction.—The habit of construct- Nest construction by myobatrachid frogs that have
ing foam nests on the surface of the water, in terrestrial aquatic foam nests is accomplished by the female, which
LIFE HISTORY
76

Figure 3-33. Foam-nest

construction by Physalaemus
pustulosas, Río Tuira, Panamá.
Note that male's feet are elevated
¡nto foam nest that is piling up on
surface of water. Photo by W. E.
Duellman.

Figure 3-34. Arbórea! foam nest

of Chiromantis petersi at the
Enzio River, Kenya. Photo by S.
Reilly.

uses her hands (Tyler and M. Davies, 1979b). Amplexus tilized as the semen, jelly, eggs, water, and rising air bub-
is inguinal, and eggs are extruded below the male's belly. bles develop into a loóse foam. The method of construc-
The female paddles with her hands in an alternating se- tion of terrestrial foam nests by myobatrachids is unknown.
quence. Each hand is brought forward, trapping tiny air Most nest-building rhacophorids construct foam nests
bubbles at the surface of the water; as the hand is drawn in trees. In some species the nests are on limbs or in forks
downward and backward the water current and bubbles of limbs, whereas in others the nests are among leaves,
are directed against the male's abdomen and between some of which may be folded around the nest. In contrast
his outstretched legs, where presumably the eggs are fer- to other frogs that construct foam nests, both the male
 Courtship and Mating
and female take an active part in nest construction. While pouch. Presumably the egg is fertilized as it is rotated at 77
n axillary amplexus, the female selects an oviposition site his cloacal opening.
above water, secretes a quantity of clear, viscous liquid,
and immediately begins beating this liquid with swimming
motions by the hindlimbs; the male makes the same Internal Fertilization
movements. As eggs, jelly, and sperm are emitted, tríese Caecilians and advanced families of salamanders all have
are beaten into a frothy mass that adheres to the branch intemal fertilization, as do a few anurans. Sperm transfer
or leaves (Fig. 3-34). During the entire process, the té- is accomplished in different ways in these groups.
nsale supports the pair by grasping a branch with her
hands. Three or four males of Chiromantís wfescens have Caecilians. Male caecilians have an intromittent or-
been observed completely or parüally amplexing a fe- gan, the phallodeum; this is the eversible phallodial por-
male, with all individuáis engaging in movements to whip tion of the cloaca, which is inserted into the female's vent
up the foam nest (Coe, 1967,1974). Múltiple males am- during copulation. Eversión is accomplished by a com-
plexing a female also have been observed in Polypedates bination of contractions of the body wall musculature and
dennysi (C. Pope, 1931). In at least some species of of the cloaca. Detailed studies on the cloaca by M. Wake
Pofypedates and Rhacophorus, a large quantity of sem- (1972) indícate that primitive caecilians (Ichthyophiidae)
inal fluid is stored in modified Wolffian ducts; this fluid, have blood sínuses that may aid in the eversión of the
in which the sperm are suspended, is discharged during phallodeum, a function also attributable to blind sacs that
amplexus and may contribute to the foam nest (Bhaduri, are present in varying sizes in many caecilians but absent
1932). However, females of some species have been in others. The phallodeum is retracted by the M. retractor
observed to construct a nest in the absence of males (C. cloacae, which originales on the posterior body wall and
Pbpe, 1931; Coe, 1974). inserts on the phallodeum. The morphology of the phal-
4. Other kinds of oviposition.—Among dendroba- lodeum is species-specific; the musculature and fibrous
ids, the absence of amplexus in some species negates connective tissues form structural features, including lon-
any continuous tactile signáis for egg deposition or ejac- gitudinal tracts possibly for the conduction of sperm, the
ulation. Observations indícate that at the time of ovipo- blind sacs probably used in phallodeal eversión, and or-
sition members of a pair face away from one another; namentation such as knobs and transverse furrows (Fig.
Ihe male emits seminal fluid on a leaf, and the female 3-35). The internal morphology of the female cloaca is
deposits eggs on the fluid. The male may even leave the less órnate than that of the male, but the pattem corre-
site before oviposition is completed (Weygoldt, 1980). sponds to that of the male. Adult male caecilians are
In some species of hylid marsupial frogs, the male takes unique in the retention of functional Mullerian ducts; the
an active part in the insertion of eggs into the pouch. posterior part of the duct is an enlarged glandular struc-
However, in Gastrotheca ovifera, while the pair is in nor- ture, the lumen of which empties into the cloaca. The
mal axillary amplexus, the female extends her hindlimbs secretions of the Mullerian glands contain fructose, acid
and raises the posterior part of her body. In this position phosphotase, and mucopolysaccharides—constituents that
with the pair tilted head down, the eggs are extruded and provide fluid for sperm transport and probably nutrition
sfide anteriorly on the female's back into the large open- (M. Wake, 1981). Subsequentto copulation, fertilization
ing of the pouch. The male's cloaca is just above the apparently takes place in the anterior part of the oviduct
opening of the pouch; presumably the eggs are fertilized (M. Wake, 1968).
as they pass below his cloaca and into the pouch (Mer-
tens, 1957). Once in amplexus the female G. ríobambae Anurans. Ascaphus truel is the only anuran known to
twists her hindlimbs so as to elévate the cloaca above the have an intromittent organ. The "tail" of male Ascaphus
ievel of the small opening to the pouch; the amplectant is a posterior extensión of the cloaca, supported in part
male produces fluid presumably containing sperm from
his cloaca and with his feet wipes this fluid over the área
between the female's cloaca and the opening of the pouch.
As the eggs are extruded, the male uses his feet to direct
the eggs along the female's back to the opening of the
pouch (Deckert, 1963; Hoogmoed, 1967). Complex in-
teractions exist between male and female Flectonotus
pygmaeus in amplexus (Duellman and Maness, 1980).
The pair is tilted head down; the female's cloaca is ele-
vated, and the male places his feet in the pouch, which
has a long middorsal opening. As an egg is extruded, it mm
slides anteriorly along the female's back; the male catches
the egg between his heels, rotates the egg next to his Figure 3-35. Intromittent organ or phallodeum of a caecilian,
cloaca, and with a pelvic thrust shoves the egg into the Geotrypetes seraphini.
LIFE HISTORY
78 that the región posterior to the sacrum is perpendicular
to the body of the female. The turgid intromittent organ
is flexed another 90° by contractions of the paired mm.
compressores cloacae, which inserí on the Nobelian rods,
and is inserted into the female's cloaca. Prior to the in-
sertion of the organ, the females legs are extended, but
after insertion her legs are drawn forward into a normal
resüng position; the period of copulaüon lasts 24 to 30
hours (Metter, 1964b). Contrary to the statement of No-
ble (1931b), Metter (1964b) noted that the engorgement
of the organ did not result in exposure of the horny spine
inside the cloacal orifice. Sperm may remain viable in the
oviducts for 2 years (Metter, 1964b).
Internal fertílizatíon is accomplished in Nectophry-
noides and Eleutherodactylus coqui and E. jasperi simply
by cloacal apposition (Grandison, 1978; Townsend et al.,
1981). Modifications of the cloacal región of male Mer-
tensophryne micranotis may be indicative of an intro-
mittent functíon (Grandison, 1980b).
Figure 3-36. Tailpiece of cloacal extensión of Ascaphus truel
inserted into cloaca of témale during inguinal amplexus. Posterior
part of body viewed from below. Adapted from a photo by R. Altig. Salamanders. Salamanders (with the exception of the
Hynobiidae, Cryptobranchidae, and Sirenidae) have a
unique method of sperm transfer: spermatophores are
Dorsal dcposited by males and picked up by females with sub-
sequent storage of sperm in the spermatheca. An excep-
tion is the single hynobüd known to produce spermato-
phores, Ranodon sibiricus, in which the female presumably
deposits eggs on a spermatophore that was previously
deposited by a male (Bannikov, 1958).
The spermatophore is a roughly conical, gelatínous
structure with a cap of sperm (Fig. 3-37); the sizes of
spermatophores are correlated with the sizes of salaman-
Lateral ders and range from 2 to 10 mm in height with about
the same dimensión for the greatest diameter of the base,
which is ovoid. The cloacal glands in the lower walls of
the male cloaca secrete a colorless, viscous material which
forms the stalk of the spermatophore; the pelvic glands
in the roof and upper walls of the cloaca secrete a whiüsh
matrix, containing polysaccharides, in which the sper-
matozoa are imbedded to form the sperm cap (Noble
and Weber, 1929). Microscopically, the matrix of the cap
mm consists of a granular and fibrous substance and plaques
of vacuolate homogeneous material concentrated near
Figure 3-37. Spermatophore of Plethodon jordani. Sperm cap is
shaded. Redrawn from Arnold (1976). the tip of the stalk; the sperm caps of Plethodon have a
covering of compact lamellated material resembling the
plaques scattered through the sperm cap (Organ and
by paired Nobelian rods, which are modifications of an Lowenthal, 1963). Observations on the deposition of
interfemoral ligament and connected with the prepubis spermatophore by plethodontids (Organ and Lowenthal,
(epipubis) by a tendinous sheet (van Dijk, 1955, 1959); 1963) indícate that during deposition the spermatophore
these rods also are present in females, and in Leiopelma is nearly horizontal in the cloaca of the male; the stalk is
and Xenopus. Immediately anterior to the cloacal orífice anterior to and slightly below the cap. Upon deposition
are proctodeal glands. The cloacal epithelium changes of the spermatophore, the male raises his vent and moves
from a mucous lining anteriorly to a cornified integument forward; this movement results in the change from nearly
posteriorly; just within the orífice are homy spines. Vas- horizontal axis to vertical axis of the spermatophore with
cularized tíssue in the intromittent organ becomes en- a resulting steep or vertical anterior surface and a more
gorged with blood making the organ turgid (Fig. 3-36). gently sloping posterior surface. The stalk is somewhat
Amplexus is inguinal, and the male arches his back so fluid and adhesive when first extruded, but quickly changes
 Courtship and Mating
» a nonadhesive gel; also the base broadens as it ad- as a dozen or so clutches may be deposited during 3 or 79
hetes to the substance. 4 days. Two genera of plethodontíds (HemidactyHum and
ki females, the spermatheca is the homologue of the Stereochilus) oviposit upside down at the edge of, or
: pelvic gland and is in the roof of the cloaca (Beau- above, static water. Some salamandrids deposit only one
nt 1933). The structure of the spermatheca is variable egg at each site. For example, Cynops, Notophthalmus,
fíobie. 1931b; Wahlert, 1953), being composed either Paramesotriton, and Triturus deposit eggs singly on leave
«oí a number of independent simple tubules lined with of aquatic plañís; Cynops pyrrhogaster deposits 1-16 eggs
eoiumnar epithelium in salamandroids or of a common each day, and a female may continué laying for about
«PC into which many such tubules open in ambysto- 50 days, producing during that time up to 324 eggs
meseóds (Fig. 3-38). The tubules are imbedded in loóse (Tsutsui, 1931). All newts carefully wrap their individual
connective tíssue, and they are located at the place of eggs in vegetation by using their hindfeet; this behavior
tbe opening of the oviducts into the cloaca. The loóse hides the egg, for adult newts will eat the eggs if a moving
connective tíssue contains many melanophores (Dent, embryo is visible. Oviposition and egg-wrapping are ac-
1970): these melanophores may provide protectíon of complished when the female is upside down.
ÉJC spermatozoa from radiatíon. The attachment of eggs to stems or leaves in midwater
The spermatophore, or only the sperm cap, is grasped prevenís the eggs from sinking into the mud on the bot-
bt the lips of the female's cloaca. The sperm cap, thus tom of ponds, where the oxygen supply is very low. Nor-
Uged in the cloaca, releases spermatozoa after it has mally Triturus and Notophthalmus oviposit only on young
fceen altered by phagocytes and leucocytes. Perhaps the leaves; experiments by Winpenny (1951) indicated that
^>erm are attracted by some secretíons of the sperma- the female has some cloacal mechanism for detecting
Éieca (Noble and Weber, 1929). The sperm arrange oxygen production, which is higher in young leaves.
•fcemselves in orderly whorls in the spermathecal tubules, 2. Lotíc sites.—Salamanders, such as Eurycea, usu-
«faere they remain until ovulation. In some salamanders ally deposit eggs on the undersides of stones in streams
sperm are stored for many months, but only for a few so that water flows past the eggs. The eggs are stalked
houzs in Ambystoma. Sperm are stored up to 2.5 years and deposited one at a time while the female is upside
m Salamandra salamandra (Joly, 1960a). In that species down and usually moving forward during deposition so
tx sperm heads penétrate the cells of the epithelial lining that the eggs are cióse together. Females of Euproctus
oí the spermathecal tubules, whereas in Notophthalmus asper have a conical cloaca and scatter their eggs among
mridescens the sperm heads are in contact with the epi- cracks and recesses in rocky streams (Gasser, 1964).
fiefium (Benson, 1968). Activity of spermatozoa in the Desmognathus hide their clutches in the banks of streams.
sxrm cap of the spermatophore is inhibited by polysac- Taricha rívuíarís, Dicamptodon, Rhyacotríton, and some
cfaarides, but these polysaccharides do not persist in the Ambystoma also lay their eggs in streams.
spermatheca. Long-term storage of the sperm in the 3. Terrestrial sites.—Terrestrial sites of oviposition are
spermatheca necessitates their obtaining nutrients, pre- characteristic of plethodontíne and bolitoglossine pleth-
sumably from the epithelial lining, but the exact mech- odontids. The eggs are all laid together and may be inde-
Mtsm is unknown. pendent of one another or attached by a central stalk to
At the time of ovulation, spermatozoa are expelled by the roof or wall of a cavity beneath a stone or log, or
contractíon of muscles surrounding the spermathecal tu- within a log. Normally the female attends the eggs.
bules, and ferülize the eggs as they enter the cloaca. In
fie Hve-bearing Salamandra, the sperm enter the ovi-
ducts. In Salamandra atra, the single egg that is fertílized
ñ each oviduct is the first to pass through the oviduct
and lodge against the oviducal opening into the cloaca;
Spermatheca
itiere it is readily reached by spermatozoa (Háfeli, 1971).
Salamanders with internal ferülizatíon have the option
Common Tube
of distributíng their eggs in space and time or placing their
eggs together and attending them. Salthe (1969) recog-
rrized three major ovipositíon sites in salamanders: open,
static water (lentic sites); hidden nesting sites associated
with running water (lotíc); and hidden terrestrial sites.
1. Lentic sites.—Most species of Ambystoma are in
this category. The female walks or swims to a twig or
stem and grasps it with her hindfeet, pressing her cloaca
K> the stem and moving forward while depositíng eggs
on the stem. As the egg capsules swell by absorbing water,
they form a clump on the stem. Only part of the ovarían Figure 3-38. Diagrammatic sagittal section of the cloaca of a
female satamander, Desmognathus fuscus, showing spermatheca.
complement is deposited at any one place, and as many Modified from Noble (19311)).
LIFE HISTORY
80 SEXUAL SELECTION monly ephemeral in that a male uses a calling station for
Sexual selection can involve one sex choosing individuáis only one night or part thereof; such is the case in Hy/a
of the opposite sex as mates (intersexual selection) or versicolor, in which a calling male emits encounter calis
competition among individuáis of one sex for access to when approached by another male (Fellers, 1979b). Males
individuáis of the opposite sex (intrasexual selection). The of other species aggressively defend territories. Size and
latter can involve either direct competition for mates or age are primary factors in successful occupation of pre-
competition for control of a critical resource. Generally ferred territories in Rana catesbeiana (R. W. Howard,
females have a greater investment in reproduction and a 1978b) and R. clamitans (Wells, 1977c, 1978b). In R.
higher certainty of parenthood than do males. Therefore, caíesbeiana, oviposition occurs in territories; larger males
females would be expected to be more discriminating in control better territories, and egg survival is highest in
their cholee of potential mates. Natural selection in both these territories (R. W. Howard, 1978a). Males of some
sexes should favor increased genetic representation in species of Centrolenella aggressively defend calling and
future generations; males tend to maximize their repro- oviposiüon sites (McDiarmid and Adler, 1974; Duellman
ducüve success by increasing the number of matings, and Savitzky, 1976); successful males of C. //eischmanni
whereas females should favor higher-quality mates. obtain many matings (Greer and Wells, 1980). However,
Althóugh an abundance of theory on sexual selection size may not be the major factor in sexual selection in
has been proposed in recent years (e.g., Trivers, 1972; these small arboreal frogs, because of the small range in
G. Williams, 1975; Burley, 1977; Emlen and Oring, 1977), size among calling males. Likewise, size is not a significant
comparatively few observatíons and experiments have factor in defense of nests in Hy/a rosenbergi (Kluge, 1981).
provided empirical evidence for sexual selection in am- Territoriality may be viewed as the defense of re-
phibians. This is not to imply that sexual selection is non- sources needed for survival and/or reproduction. As em-
existent in most amphibians, but rather that biologists are phasized by Wells (1977a), the attachment to a fixed site
only now becoming aware of the phenomena and that will be advantageous if it gives the occupant exclusive or
much careful work needs to be done. The limited infor- priority access to limited resources. Females may be the
matíon on a few selected species of amphibians suggests limited resource, and they usually are not defendable
that complex sexual interactions, some of which are den- except by guarding during amplexus or courtship (see
sity-dependent, support Berven's (1981:707) generalized the later section: Sexual Defense).
contention: "The major mechanism hypothesized that Aggressive behavior related to site-specific territoriality
underlies patterns of sexual selection is that discriminating has been documented in a few terrestrial salamanders—
females control the reproduction of indiscriminate males." Aneides aeneus (Cupp, 1980) and two species of Pleth-
odon (R. Jaeger and Gergits, 1979)—and has been re-
ported in aquatic cryptobranchoids having external fer-
Mate Selection tilizatíon and defending ovipositíon sites—Hynobius
Berven (1981) postulated four possible explanatíons for nebulosas (Thorn, 1962), Cryptobranchus alleganiensis
the patterns of anuran maüng behavior: (Bishop, 1941), and Andrias japónicas (Kerbert, 1904).
Physical combat between male frogs frequentiy is preceded
1. Male-male competition, whereby males are by agonistic vocalizatíons (see Chapter 4); some frogs
competing for females, and the larger males also have postural or visual displays (Table 3-2). Terri-
are competitively superior to the smaller males. torial males of Rana catesbeiana and R. clamitans main-
2. Female choice, whereby females choose larger tain high, inflated positions in the water (Emlen, 1968;
(or better) males. Wells, 1978b). Territorial males of Co/ostethus inguina/is
3. Size-assorüve mating, whereby females choose display their white throats (Wells, 1980a), and territorial
males of nearly equivalent or proporüonately females of C. collaris and C. herminae display their bright
larger body size. yellow throats (Durant and Dole, 1975; Sexton, 1960).
4. Male choice, whereby males discrimínate against These and other dendrobaüds usually assume an erect
smaller females. posture with stiffened limbs when challenging intruders;
a similar posture has been observed in male Centrole-
Male-male competition for mates may be by means of nella (Wells, 1977a). Physical combat in anurans may be
scramble competition, in which males actively search for simply a butting of the intruder by the territorial male, as
mates and larger males tend to domínate the search área, in Pseudophryne (Pengilley, 1971). More physical bouts
forcing smaller males into áreas where they are less likely include grappling or wrestling, as in dendrobatids and
to find females. This form of sexual selection is especially Centrolenella (Duellman, 1966; McDiarmid and Adler,
prevalent among anurans that have short, intense breed- 1974; Duellman and Savitzky, 1976). In frogs that have
ing seasons, such as Rana sylvatica (Wells, 1977b, c; R. prepollical spines, these bouts may result in injuries or
W. Howard, 1980; Berven, 1981). fatalities (B. Lutz, 1960,1973; Rivero and Esteves, 1969;
Althóugh many male anurans that have prolonged Kluge, 1981). Duellman and Trueb have observed biting
breeding seasons maintain territories, these are com- in the Hy/a microcephala; biting also was reported for
Tabla 9-2. Territorial Italmvlnr In Anurant
Territorial bahavlor

Hymenochirus boettgeri* 3 Underwater calling site G. Rabb and M. Rabb (1963a)

Pipa carvalhoi* 3 Underwater calling site Weygoldt (1976a)
Pipa pipa* 3 Underwater calling site G. Rabb and M. Rabb (1963b)
Pipa pama* 3 Underwater calling site G. Rabb (1969)
Limnodynastes dumerifí ó Pool or burrow Clyne (1967)
Pseudophryne bibroni 3 Terrestrial burrow PengiUey (1971)
Pseudophryne corroboree 3 Terrestrial burrow PengiUey (1971)
Pseudophryne dendyi 3 Terrestrial burrow PengiUey (1971)
Eleutherodactylus coqui 3, 9 Tree hole Drewry (1970)
E/eutherodacty/us hedricki 3 Tree hole Drewry (1970)
Eleutherodactylus urichi 3 Tree hole Wells (1981b)
Leptodactylus bolivianus 3 Foam nest in water Sexton (1962)
Leptodactylus melanonotus 3 Under rocks near water Brattstrom and Yamell (1968)
Leptodactylus pentadactylus 3 Margin of pond Rivero and Esteves (1969)
Colostethus collaris 3, 9 Rocks in stream Durant and Dole (1975)
Co/osteíhus inguina/is 3, 9 Rocks in stream Wells (1980a)
Colostethus trinitatus 3, 9 Rocks in stream Wells (1980b)
Dendrobates granuliferus 3 Logs, leaves, stems Goodman (1971); Crump (1972)
Dendrobates histrionicus 3 Logs, leaves, stems Silverstone (1973)
Dendrobates pumilió 3 Logs, plants, ground Duellman (1966); Bunnell (1973);
Weygoldt (1980); McVey et al. (1981)
Hyla faber 3 Excavated nest Lutz (1960)
Hyla parda/is 3 Excavated nest Lutz (1973)
Hyla rosenbergi 3 Excavated nest Kluge (1981)
Pachymedusa dacnicolor 3 Burrow Wiewandt (1971)
Centrolenella fleischmanni 3 Plant over stream McDiarmid and Adler (1974); Greer and
Wells (1980)
Centrolenella griffithsi 3 Plant over stream Duellman and Savitzky (1976)
Centrolenella valerioi 3 Plant over stream McDiarmid and Adler (1974)
Rana catesbeiana 3 Vegetated área of pond Emlen (1968); Howard (1978a)
Rana clamitans 3 Margin of pond Wells (1978b)
*Captive animáis. Based on Wells (1977a) with addifions.
LIFE HISTORY
Eleutherodactylus caqui (Reyes Campos, 1971) and for tory, tactíle, and visual cues provided during early stages
Phyí/odyfes luteolus (Weygoldt, 1981). of courtship; escape behavior by a female may indícate
Diurnal, terrestrial dentrobatids may defend all-pur- that she is not physiologically ready to mate or that she
pose territories that include feeding sites, shelter, and ovi- is not receptive to a particular male. For example, female
position sites (Wells, 1977a, 1980a). Holes in trees that newts (Triturus) seem to prefer large males with well-
are used for shelter and ovipositíon sites are defended developed crests (Halliday, 1977).
by some species of Eleutherodactylus (Drewry, 1970). In Lek behavior involves a communal display área where
all of these groups, territorial behavior, typical of males, males congrégate for the solé purpose of attracting and
is characteristic of females of some species. courting females which come for breeding (Emlen and
Calling sites and courtship sites are defended by many Oring, 1977). Males do not control females directly, ñor
species of frogs. These include diumal terrestrial dendro- do they control resources, such as oviposition sites, needed
batids, arboreal hylids, semiaquatic ranids, and aquatic by the females. Lek behavior has been proposed for the
pipids. bullfrog Rana catesbeiana (Emlen, 1976), but R. W.
Females may choose larger males; large size and greater Howard (1978a) showed that males controlled territories
age are indicative of rapid growth rate and/or longevity, in which the females oviposited. Likewise, even though
both of which are good indicators of fitness. Gravid fe- frogs, such as Hy/a rosenbergi and some species of Cen-
male Uperoleia rugosa mate only with calling males and trolenella, congrégate for breeding, individual males de-
usually choose the largest male available (Robertson, fend calling sites that are also oviposition sites. Thus, in
1981). Comparison of sizes of mated versus nonmated most amphibian mating systems, males seem to control
males in Bufo quertícus (Wilbur et al, 1978) and Hy/a either females or oviposition sites; lek behavior has yet
marmorata (J. Lee and Crump, 1981) revealed that mated to be demonstrated in amphibians.
males were larger; these results were interpreted as fe-
male choice of larger mates. How do females select larger Mating Success
mates? Vocalizaüons may provide information about the In most amphibian mating systems, the operational sex
size of the calling male (see Chapter 4). Females of Phys- ratio (number of ready malesinumber of receptive fe-
ataemus pustulosus discriminate against higher funda- males at any given time) is highly skewed in favor of
mental frequencies of the cali and therefore choose larger males. Ratios of seven or eight males per female are not
males, which cali at lower frequencies (M. Ryan, 1980). uncommon among explosive breeders, whereas the pro-
They also tend to choose males that have more complex portion of females may be higher in long-term breeders.
calis (Rand and M. Ryan, 1981). However, one notable exception is known; in Dendro-
Females of Hy/a rosenbergi apparently choose mates bates auratus, males are occupied by attending clutches,
by the location of the nests (calling statíons), preferring so the number of receptive females may exceed the num-
males that cali from groups rather than isolates (Kluge, ber of available males (Wells, 1978a).
1981). Furthermore, females enter the nests of calling The variance in mating success generally is much lower
males and bump the males; if a male jumps out of the in males than in females. The measurement of mating
nest the female will leave. Kluge (1981) interpreted these success in salamanders is difficult, because in most spe-
observations as female choice of male quality. A male cies courtship and oviposition take place at widely sep-
calling as part of a group and also maintaining his posiüon arated intervals; furthermore, females may pick up more
when bumped can be assessed as an individual capable than one spermatophore, so male parentage cannot be
of defending his nest, an importan! attribute in that sur- determined. The number of spermatophores deposited
vival of eggs and tadpoles depends on his ability to re- per courtship and the amount of time devoted to each
main at the nest for several days. courtship have been used as a measure of mating success
Size-assorüve maüng presumably involves female choice and male investment in salamanders (Amold, 1977). As
of a mate that is of a size that will not interfere with her examples, Ambystoma deposit many spermatophores per
movements during oviposition but will be effective in fer- courtship and invest only a few minutes in each sper-
tilizing the eggs. Positive correlatíons between sizes of matophore; A. maculatum deposits as many as 81 sper-
mated pairs have been reported for Bufo bufo (N. Davies matophores per courtship with an average investment of
and Halliday, 1978), B. americanus (L. Licht, 1976), and 1.4 minutes per spermatophore (Arnold, 1976). Sala-
Triprion petasatus (J. Lee and Crump, 1981), but there mandrids usually deposit only 1-4 spermatophores per
is no evidence of active female choice in any of these courtship, whereas the modal number is 1 in plethodon-
species. Males also may choose females by size; for ex- tids, in which the temporal investment may be 1-5 hours
ample, males of Rana syhatica prefer larger females per courtship (Arnold, 1977). Lengthy courtships tend to
(Berven, 1981). result in a higher probability of the female discovering
There are even fewer observations and interpretations and recovering a spermatophore (Fig. 3-39).
of mate choice in salamanders. Mate choice by male and Although the data are extremely limited, some general
female salamanders may result from the complex olfac- patterns of mating success seem to be evident (Table 3-
 Courtship and Mating
3). In explosive and short-term breeders, such as Rana 83
sytvatica, Bufo typhonius, and Pseudacris triseriata, var- to- c? 8
ance in male mating success is low, whereas in species
mlth longer breeding seasons and especially those species ar -8" B
exhibiting male teritoriality, chances for a successful mat- 5 6- 9 *• 41
F

ng and múltiple matings are higher. However, some males 2 ' A \ ? J

sáD obtain no mates. £.4-
•
The factors responsible for male mating success in anu- .2-
lans are not well understood. Most Hyla versicolor calling ?
frrxn perches, where there is the least habitat inteference
with the propagation of the cali, are more likely to obtain Relative Investment per Spermatophore
a male than mates calling from less desirable perches
Figure 3-39. Success of individual spermatophores as a function
(FeDers, 1979b). Calling and oviposition sites, as well as of relative mate investment per spermatophore. Open circles
Éie number of nights of calling, are positively correlated indícate probability of discovery by the female; solid circles indícate
probability of recovery of sperm cap by female. A. Ambystoma
«¡un mating success in Centrolenella fleischmanni (Greer maculatum. B. Ambystoma figrinum. C. Range of variation in
and Wells, 1980). Males of Hyla chrysoscelis that spent Trítums cristatus, helvéticas, and vulgaris. D. Plethodon jordani.
more nights calling obtained more matings than those Modified from Arnold (1977).
fíat were at the breeding pond only a few nights; fur-
áiermore, the probability of a male obtaining a mate in-
cxeased late in the season when few males were at the successful matíng prior to interference by a rival male.
pond (Godwin and Roble, 1983). Quality of males' ter- Prolonged amplexus in anurans may be a strategy for
ritories clearly influences mating success in Rana cates- monopolizing a female, especially if pairing takes place
bdana and R. clamitans (R. W. Howard, 1978b; Wells, before ovulation (Wells, 1977a). Amplexus takes place
1977c). Significantly more matings were obtained by more at the breeding site and may last for 12 days in Rana
aggressive males in the territorial Hyla rosenbergi (Kluge, temporaria (Geisselmann et al., 1971) or 14 days in Bufo
1981). With the exception of scramble competition for bufo (Heusser, 1963). In Atelopus oxyrhynchus, pairing
females in explosive breeders, in which larger male size may occur before the frogs reach a breeding site, and
sometimes is advantageous, the mating success of a given pairs may be in amplexus for periods up to 125 days
male may depend on a combinatíon of several factors— (Dole and Durant, 1974a). Observations of unmated males
time of arrival at a breeding site, duration of stay at the attempüng to dislodge amplecüng males indícate that most
breeding site, territorial behavior, aggressive behavior to- mated males maintain amplexus and therefore are effec-
ward other males, effectiveness of visual displays, and in tively monopolizing the mated female.
anurans the choice of a calling site and perhaps the qual-
íy of the cali. Sexual Interference
Several kinds of behavior by male amphibians are di-
Sexual Defense rected at obtaining maüngs at the expense of courtship
Intraspecific competition among males for mates is known investment by another male. Arnold (1976, 1977) re-
in many amphibians. This is most evident in the calling viewed sexual interference in salamanders and noted that
behavior with respect to territories and encounters in sexual interference can be accomplished by stealing a
anurans (see Chapter 4). However, nonvocal behavior female, disrupüng the spermatophore deposiüon of a ri-
at breeding sites involves ways of monopolizing females. val male, covering the spermatophores of rival males, or
Males of Rhyacotriton olympicus and several plethodon- duping rival males into unprofitable spermatophore dep-
tid salamanders (species of Desmognathus, Eurycea, ositions.
Plethodon, and Pseudotriton) are known to bite and Spermatophore covering is common in Ambystoma.
sometimes chase males that interfere with courtship (Ar- Many males vie for one female, and males deposit many
nold, 1977). Among aquatic salamanders, males may spermatophores. In species such as A. maculatum, in
shove females away from other males, as in Ambystoma which courtship involves only nudging, males not only
tígrinum (Arnold, 1976), or in cases in which the male deposit spermatophores on top of other spermatophores,
actually captures the female, he swims away from rival including their own, but nudge females trying to pick up
males and carnes the female with him—A. laterale (Sto- spermatophores and rival males depositing spermato-
rez, 1969), Taricha, and Pleurodeles (Arnold, 1977). The phores. Sometimes in A. maculatum a male has been
rapid courtship and múltiple spermatophores of some observed to follow another male that is depositing sper-
Ambystoma (e.g., A. maculatum) may be interpreted as matophores and then to cover each one with a sper-
a form of sexual defense (Arnold, 1976). By producing matophore of his own. In some instances a male has
many spermatophores quickly in the presence of a re- been observed to circle behind his follower and deposit

'
ceptive female, the male is increasing his chances of a another spermatophore on top of that deposited by the
Table 3-3. Maüng Success in Male Anurans"

Number of matings Number of Percent of Matings per Matings

Seasons Number successful males successful per
Species oí data of males 0 1 2 3 4 5 6 7 8 9 matings successful mate male
Physalaemus pustulosas 1 185 119 43 16 2 4 — 1 — — — 103 35.6 1.56 0.557
Bufo amerícanus 1 129 93 33 3 — — — — — — —
39 27.9 1.08 0.302
Bufo bufo 1 73 58 14 1 —1
—
— — — — —
16 20.5 1.07 0.219
Bufo canoras 4 795 595 165 34 — 236 25.2 1.18 0.297
— — — — —
Bufo exul 2 1288 952 295 38 3 — —
— — — — 380 26.1 1.13 0.295
Bufo typhonius 1 160 98 61 1 — — — — — — 63 38.8 1.02 0.394
1 124 —2 —
Hyla chrysoscelis* 81 33 8 —
— — — —
55 34.7 1.28 0.444
Hy/a rosenbergí 2 95 43 24 14 4 7 1 2 109 54.7 2.10 1.147
Hyla versicolor 1 35 26 8 1 —
— —
— — — — 10 25.7 1.11 0.286
Pseudacris triseriatcf 2 442 366 75 1 — 77 17.2 1.01 0.174
—7 — — — — —
Centrolenella colymbiphyllum 1 101 27 35 22 4 3 1 1 1 — 152 73.3 2.05 1.505
Centrolenella fleischmannid 1 14 1 1 1 4 3 1 — 1 — 1 59 92.9 4.54 4.214
Centrolenella ualerioi 1 56 15 9 9 13 5 4 1 — — — 112 73.2 2.73 2.000
Rana catesbeiana 3 93 45 24 12 8 2 — 1 1 — — 93 51.6 1.94 1.000
Rana clamitans 2 46 21 17 6 1 1 — — — — 37 54.3 1.48 0.804
—
—
Rana syluatica 1 345 289 54 3 —1 — — — — — 60 19.1 1.07 0.174
Rana temporaria 1 33 16 15 1 — — — — — — 20 51.5 1.18 0.606
"Based on tabulatíons in Kluge (1981), except as noted.
bGodwin and Roble (1983).
cRoble (pers. comm.).
dGreer and Wells (1980).
 Courtship and Mating
follower; thus a triple spermatophore results (Arnold, one natural observation of H. ebraccata, the satellite male
1976). achieved amplexus (Miyamoto and Cañe, 1980b).
Duping of males is known in Ambystoma tigrinum, In the species of Hyla and Pseudacris nigrita, there is
Desmognathus ochrophaeus, Ensatina eschscholtzi, no size difference between calling and satellite males.
Pseudotriton ruber, and four large species of Plethodon Furthermore, in H. cinérea, H. chrysoscelis, and P. ni-
(Organ and Organ, 1968; Arnold, 1976, 1977). During grita, individual males changed strategies from calling to
the aquatic courtship of A. tigrinum, the female follows satellite behavior or from satellite to calling behavior on
the male and nudges his cloaca with her snout. The con- different nights or on the same night (Perrill et al., 1978;
tinuation of his behavior and deposition of a spermato- Godwin and Roble, 1983; S. N. Roble, pers. comm.).
phore depend on the continua! nudging of his cloaca. A
rival male can replace the female and have the female Reproductive Interference
follow him. The original male deposits a spermatophore, Interference with the development of the eggs or young
which is covered by the spermatophore of the interfering is another form of intraspecific compeütion that may en-
male; if the female picks up a spermatophore, it is the hance the reproductive success of one individual at the
one deposited by the second male. Males intrude during expense of another. Conspecific oophagy is common
the tail-straddling walk in plethodontíd courtship and dupe among female plethodontid salamanders that have ter-
other males into depositing spermatophores. restrial nests; females attend their own eggs and drive off
Sexual interference in anurans involves the association potential predators, including conspecific females. Some
of silent males with calling males. This satellite behavior newts (Notophthalmus and Taricha) eat conspecific eggs
or "sexual parasitism" has been reported for various spe- (J. Wood and Goodwin, 1954; Kaplan and P. Sherman,
cies of Bu/o, Hyla, Pseudacris, Rana, and Gastrophryne 1980). Possibly because of this behavior, the eggs of
(Axtell, 1958; L. Brown and Pierce, 1967; Wells, 1977c, newts are concealed singly or in small clumps amidst
1978b; R. W. Howard, 1978a; Pemil et al., 1978; Fellers, aquatic vegetation. Moreover, it is not known if individ-
1979a, 1979b; Miyamoto and Cañe, 1980b; Roble, pers. uáis recognize their own eggs, so oophagy in newts might
comm.; Godwin and Roble, 1983). Satellite males sit be indiscriminate cannibalism.
quietly near calling males and commonly maintain a low The eaüng or destruction of eggs and larvae in con-
posture, presumably making themselves inconspicuous specific clutches has been documented in two species of
to the calling males, which may chase them away. Two Dendrobates. Males of D. pumi/io are territorial and at-
or three satellites have been observed with one calling tend egg clutches. When males find an unattended clutch
male in several species. fertilized by another male, they eat the eggs, of if the
Two hypotheses have been proposed for this satellite eggs are hatching, the male sits in a clutch; when a tad-
behavior: satellite males are waitíng for calling sites or pole climbs onto his back, he carries it to a bromeliad
tentones to become available after the calling male mates; axil or crevice and leaves it (Weygoldt, 1980). Because
and satellite males intercept females as they move toward tadpoles are dependen! on eggs provided by a female
calling males (Wells, 1977b). These hypotheses are not for food, those tadpoles transported to sites unknown to
mutually exclusive. The former seems to account for the the female probably will not survive. Females of Den-
satellite behavior in Hyla versicolor, in which there is a drobates auratus, lehmanni, and hisírionicus have been
positive correlaüon between cali site and mating success observed to eat or destroy eggs in other females' clutches
(Fellers, 1979b). In the territorial species Rana cates- (Wells, 1978a; H. Zimmermann and E. Zimmermann,
beiana and R. clamitans, satellite males are smaller than 1981).
calling males and also seem to await the vacancy of a
territory. Two of 73 maüngs in R. catesbeiana were by
satellite males (R. W. Howard, 1978a). Males of the small EVOLUTION OF MATING SYSTEMS
Australian myobatrachid Uperoleia rugosa establish ter- Both males and females face the same basic problem of
ritories in grass adjacent to ponds. Satellite males do not having to form mating relationships in a way that best
intercept females approaching calling males, but the sat- enhances their reproductive success. However, the mat-
ellites may take over a calling site when a female carries ing relaüonship yielding maximal success is not neces-
the former territory-holder to an oviposition site, or sat- sarily the same for both sexes. In most amphibians, males
ellites may replace territory-holders that have become compete among themselves for maüng opportunities, and
physically weakened after maintaining their territories for females assume noncompetitive roles, mating with win-
several weeks (Robertson, 1981). Convincing experi- ning males or choosing among courüng males. Males
mental evidence for successful interception of females by usually are not discriminating in their choice of prospec-
satellite males is available for two species of Hyla. In 13 tive mates, whereas females often are highly selective in
of 30 field experiments with the reléase of a gravid female choosing their mates. Male competition and female choice
near a calling male-satellite associaüon in H. cinérea, the are the consequences of the different costs to each sex
satellite successfully intercepted the female (Perrill et al., to produce offspring. Ova are energetically more costly
1978). In three of seven similar field experiments and to produce than sperm; therefore, female reproductive
LIFE HISTORY
"" output is limited by resource availability and time con- be measured energetícally (Crump and Kaplan, 1979;
straints, not mate availability. Males generally produce Kaplan, 1980b). However, little information exists on the
many more sperm than needed to fertílize all of the eggs energy expenditures required for calling and courtship
produced by available females. Thus, the availability of actívities. Male salamanders that produce large quantíties
receptive females is limiting, and males normally compete of spermatophores per courtship deplete their sperma-
to fertilize as many eggs as possible. tophore supply after a few days, whereas plethodontids,
Males that exhibit paternal care increase their invest- which produce only one spermatophore, or rarely two,
ment in reproduction, and it is significant that clutch sizes per courtship can continué production and therefore po-
in such species are small. Also, salamanders that have tentially successful courtships for many weeks (Arnold,
lengthy courtships tend to produce few spermatophores. 1977). Moreover, males require energy to develop sec-
Similarly, male frogs that have a large investment in ter- ondary sexual characteristícs and to defend territories.
ritorial defense tend to have relatively high reproductive Males of explosive-breeding anurans usually have empty
success, but some individuáis are unsuccessful. stomachs after one day at the breeding site; apparently
Male mating strategies are adaptations to environmen- all efforts are directed toward matíng, and these frogs
tal conditions, primarily the length of the breeding sea- generally do not feed during the brief breeding season.
son. Explosive breeding involves a short, synchronous However, males that advertíse for mates for many weeks
burst of breeding acüvity once or a few ümes each year. or months must acquire nutrition during this tíme. Prob-
This is characteristic of many températe species that breed ably frogs that are absent from a breeding site for a few
in the spring, as well as tropical anurans that breed pri- nights before resuming calling are taking time off for feed-
marily in ephemeral aquaüc situatíons. However, some ing. Because most anurans have a sit-and-wait feeding
tropical species, such as Bu/o typ/ionius, are explosive strategy, males of prolonged breeders may obtain some
breeders and do not utílize ephemeral habitats (Wells, food at their calling sites; probably this is especially im-
1979); the selective advantage of synchronous oviposi- portant to territorial species. A male that can obtain suf-
üon in such species may be the satiation of predators by ficient food in his territory can defend the territory and
larvae and thus the survivorship of some offspring (Wal- advertise consistently, thereby increasing his chances for
ters, 1975). On the other hand, prolonged breeding may reproductive success. But even territorial species may lose
last several months in températe climates to all year in weight during the breeding season, as was noted in Rana
the tropics. clámitans by Wells (1978b).
At high densities males of explosive-breeding anurans With the exception of those species of frogs in which
acüvely search for mates, even though many males are calling males are larger and satellite males are smaller
advertising vocally and attracting females to the breeding and subordínate, the satellite behavior of males and their
site. At high densitíes there is intense male-male com- switching of roles may be a mechanism whereby a male
peütíon for mates, and size and aggressiveness of males can conserve energy and still possibly obtain a mate.
are importan! factors in matíng success. At lower densities In summary, the matíng systems of amphibians are
males of explosive-breeding anurans usually are dis- highly complex, involving simple to elabórate courtship
persed at the breeding site; physical competítion among behavior. Some behavioral traits coincide with reproduc-
males is reduced because advertisement calis are more tíve and morphological evolutionary trends. Courtship
effective in attracting a female to a particular male. Thus, behavior in salamanders evolved in diverse ways once
at low densities the mating strategies of explosive-breed- salamanders developed spermatophores, and some of
ing anurans are more like those of prolonged breeders. the behaviors are phylogenetically related—tail and cloa-
Among anurans, the establishment and defense of ter- cal nudging in ambystomatíds and the tail-straddling walk
ritories is associated only with prolonged breeders. In in plethodontids. Likewise, amplectic position in anurans
these frogs, matíng success depends not so much on the is associated with the general phylogeny of the group,
search and scramble competition for females but on the but there are exceptíons. Within both salamanders and
attraction of females to the male's territory- Thus, in pro- anurans, specialized courtship and matíng behaviors are
longed breeders, female choice is a major factor in mate associated with certain specialized modes of reproduction
selection. The amount of time that a male defends a and in some species involve complex interactions of both
territory contributes to the probability of múltiple matings. sexes (e.g., some pipids, foam nest-builders, some mar-
However, maintenance of a territory by an advertising supial frogs). Likewise, within both groups, mating strat-
male does not necessarily ensure reproductive success. egies differ with densitíes and duration of the breeding
For example, 43 of 95 male Hyla rosenbergi that called season. Existíng knowledge of courtship and mating be-
from defended nests obtained no matings, whereas 28 havior and its evolutionary implicatíons in amphibians is
males mated more than once (Kluge, 1981). sufficient to titillate the imaginatíon for much further ob-
The energetic aspects of courtship and matíng remain servaflon and experimentation.
essentíally unknown. The strictly reproductíve factors can
 CHAPTER 4
Frogsfeel physicaljoy and ey.press tt in
song.
Mary C. Dickerson (1906)

s. "ound producüon by animáis is primarily a method

of advertising the presence of one individual to others of
the same species. Vocalization is most common in ani-
mechanisms (Maslin, 1950; Neill, 1952; Wyman and
Thrall, 1972; L. Licht, 1973; J. Davis and Brattstrom,
1975; Brodie, 1978) or as an aid in orientation (Gehl-
máis that have low-density dispersa! and that jump or fly, bach and Walker, 1970). The limited informatíon on sound
thereby leaving no continuous trail to be followed by production in salamanders seems to associate vocaliza-
chemosensory means. Thus, among the insects, sound tion with defense (Chapter 10).
production is characterisüc of cicadas and (by stridula- This chapter is devoted to anurans, most species of
tion) orthopterans. Among vertebrates, vocalization is which have well-developed vocal structures capable of
highly developed in anurans, birds, bats, primates, ce- producing a variety of sounds that serve to attract mates,
taceans, and dolphins. In the anurans and birds the pri- adverüse territories, or express distress. The complex suite
mary purpose of vocalization is adverüsement, but pas- of morphological and behavioral characterisücs associ-
serine birds show a further diversity of behavioral responses ated with sound production seems to have evolved con-
associated with various kinds of vocalizations. The high- comitantly with saltatorial locomotion. Because the force-
frequency sounds emitted by bats serve in echolocatíon pump breathing mechanism is an integral part of the sound
and, probably secondarily, as advertisement, whereas production system (see Chapter 14), there is an oblígate
primates and marine mammals have complex vocal com- mechanical and physiological interdependence between
munication systems. the breathing mechanism and the vocal system. The
Sound production is quite limited in salamanders presence of structures in the middle ear of Permian dis-
(Maslin, 1950; Bogert, 1960) and has been reported in sorophids (DeMar, 1968) and Jurassic leiopelmatid frogs
only two caecilians—Geotrypetes grandisonae (Largen et (Estes and Reig, 1973) that are essenttally equivalent to
al., 1972) and Dermophis mexicanus (Thurow and Gould, those of modern anurans suggests that vocalization may
1977), but clicking sounds are produced by at least two have existed in protolissamphibians, as well as in primi-
other caecilians—Ichthyophis and Siphonops (C. Gans, tive anurans.
pers. comm.). The various soft squeeks produced by some Early reviews of anuran vocalizations (Bogert, 1960;
plethodonüd salamanders, low whistles by Siren and W. Blair, 1963; Paillette, 1971) were concemed primarily
Amphiuma, and a variety of sounds (barks, clicks, squeaks, with the evoluüonary significance of vocalization at pop-
whistles) in P/eurode/es, Taricha, Dicamptodon, and Am- ulation and species levéis; Straughan (1973) provided an
bystoma have been interpreted variously as defense overview of evoluüon of vocalization in anurans. W. Mar-
87

"i*!!
LIFE HISTORY
88
Common \e i
Destination Source
cíor ijFrog Advertisement ¡ d Frog
r^\i i

Message Message

Decoder Encoder
Ear/Brain Noise Brain

Calis of
Receiver Conspecifics and Transmitter
Ear Other Species; Vocal
Abiotic Sounds Apparatus

Channel
-Signal- -Signal-
Air or Water

Figure 4-1. Components of a

communication system. Anuran Selective
counterparts of each component are Environmental
shown ¡n lightface lettering. Modified Absorbtion
from Littlejohn (1977).

o
O Harmonios
c ij
Pulses

Domtnant frequency

Fundamental frequency

Fignre 4-2. Audiospectrogram of a note from

the advertisement cali of the hylid frog Triprion Duration (in seconds)
petasatus showing acoustic components.

tin and Gans (1972), Gans (1973), and R. Schmidt (1973) model requires a transmitter to emit sound and a receiver
provided insights into the mechanisms and control of vo- to process and respond to the signal (Fig. 4-1). By defi-
calizations. More recent syntheses by Wells (1977a, 1977b) nition, sound is mechanical radiant energy that is trans-
and Littlejohn (1977) emphasized the evolutionary and mitted in longitudinal pressure waves in a material mé-
ecológica! interactions at the individual level. dium. This mechanical perturbation of the environment
is the signal that the receiver processes.
Acoustic parameters of frog calis can be described by
ANURAN COMMUNICATION SYSTEM analyzing tape recordings of the vocalizations with elec-
A model communication system proposed by Shannon tronic sound analyzers. This equipment produces visual
and Weaver (1949) was used by Littlejohn (1977) to representations of the calis on an oscilloscope or as os-
explain the behavior significance and physical attributes cillographs or audiospectrographs (Fig. 4-2). Intensity
of vocalization among anurans. In its simplest form, the (loudness) is measured in decibels (dB) on a peak-sound-
 Vocalization
lewá meter. The various components of anuran vocali- quencies (R. Wiley and D. Richards, 1978). Thus, Little- 89
«óons are as follows: john (1977) suggested that transmission at lower fre-
quencies (<4000 Hz) is most effective for anurans. By
1. Cali or cali group is the entire assemblage of comparison, the range of máximum acoustic sensitivity
acoustic signáis produced in a given se- in humans is 800-2500 Hz.
quence. This may be a single note, a series Body size and relative size of the vocal apparatus have
of idenücal notes, or groups of notes having an effect on the acoustic properties of the calis. W. Blair
different acoustic characteristics. (1964) demonstrated that small species of toads, Bufo,
2. Cali rate is the frequency of producüon of calis have higher dominant frequencies than larger species. In
or cali groups; usually these are measured in two toads, B. americanus and B. woodhousn fowlerí, in-
calis per minute. traspecific (but not necessarily intrapopulational) size dif-
3. A note is a given individual unit of sound, ferences are correlated with acoustic properties of the
whether a short, single pulse or a long series calis; larger individuáis have higher pulse rates, longer
of pulses (trill). calis, and lower dominant frequencies (Zweifel, 1968). A
4. Note repetition rate is the frequency of pro- highly significant correlation exists between dominant fre-
duction of notes in a multinote cali and is quency and body length among 81 species of Papuan
measured in notes per second. frogs (Menzies and Tyler, 1977) and 39 species of neo-
5. Putees are emphasized energetic impulses in tropical hylid frogs (Duellman and Pyles, 1983). There is
the temporal spectrum of a note. In some long a significant negative correlation between body length
notes, such as the trills of toads, individual and fundamental frequency of the secondary notes (chuck
pulses are audible to the human ear. Some cali) of the leptodactylidPhysa/aemuspustu/osus (M. Ryan,
notes are unpulsed. 1980a). Moreover, an allometric relationship exists be-
6. Putee rate is the number of pulses per second tween larynx size and body size in Bufo; those species
or millisecond. with proportionately large larynges have calis with lower
7. Spectral frequency or spectral bandwidth is the dominant frequencies (W. Martin, 1972). In general, small
pitch of the cali. The sound emanating from frogs tend to cali at higher frequencies and to have re-
a frog has a spectrum of frequencies, measured duced auditory sensitivity; cali frequencies of most anu-
in Hertz (Hz). In well-tuned notes, the spec- rans are below 5,000 Hz (Loftus-Hills, 1973).
trum is divided into distinct harmonics, which
are masked but nevertheless present in poorly
tuned notes. The oscillations resulting from air MECHANISMS OF SOUND
passing over the vocal cords and causing them PRODUCTION AND RECEPTION
to víbrate at a frequency primarily dependent
on the mass and tensión of the cords is the Sound Production Apparatus
first (lowest-pitched) harmonic, usually re- In most tetrapods the laryngeal apparatus, or voice box,
ferred to as the fundamental frequency. The is the structure that produces sound, and in general can
frequency of sound resulting from the reson- be visualized as a cartilaginous capsule (larynx) that houses
ating of the fundamental frequency (or one vocal cords. The laryngeal apparatus is located between
of its harmonics) with greater emphasis than the lungs and the buccal cavity; air leaves the lungs and
any other frequency is the dominant fre- passes over flaps and strings of connective tissue (vocal
quency. This frequency is always a múltiple cords) and their associated cartilages, causing these struc-
of the fundamental frequency. In some cases tures to víbrate. The vibration induces pulsation of the
two or more harmonics may be emphasized. air column that is perceived as sound. The quality of the
sound depends on several factors: the masses of the vi-
The acoustic signáis generated by air passing over the brating structures; their tensions; and the nature of the
vocal cords and usually resonated by a vocal sac are resonating chambers, through which the sound travels
emitted into the environment—air, water, soil, each of before leaving the body, and the way the impedance is
which has a characteristic impedance to sound transmis- matched to the external environment.
sion. The signáis of most anurans are transmitted by air. Although there is considerable diversity in the structure
Reduction of transmission range is affected by several of the anuran larynx (see Trewavas, 1933; W. Martin,
environmental factors. For each doubling of transmission 1972; Schneider, 1977; Drewry et al., 1982, for more
distance, the attenuation of sound waves, irrespective of comprehensive accounts of variation), in most frogs, such
frequencies, is at the rate of 6 dB; thus, the sound pres- as Bufo valliceps (described in the section: Sound Pro-
sure level is reduced by half (inverse-square law). More duction), the larynx is composed of two arytenoid carti-
acoustic energy is absorbed by the atmosphere at higher lages. Together, these cartilages form a compressed,
frequencies, higher temperatures, and lower humidities. hemispheric structure, the lumen of which houses the
Sound waves also are attenuated by the substrate and vocal cords; one vocal cord is associated with each ary-
vegetation; these have most notable effects at higher fre- tenoid cartilage. The arytenoid cartilages are poised within
LIFE HISTORY
90
posterior

—Esophageal process
M. sphincter anterior
M. sphincter posterior — Arytenoid cartilage
Cricoid cartilage
Lateral process M. dilatator laryngis
Lung
M. hyolaryngeus Hyale
Bronchial process
Posteromedial process

Hya le Hyoid
píate
Posterolateral process

Alary process-

ventral
Figure 4-3. Isometric diagram of an
anuran hyolaryngeal apparatus.

a ring of cartilage (cricoid cartilage} at their common base. Upper jaw

The ring, together with its processes, the larynx, and as- Opening of
sociated musculature, composes the laryngeal apparatus internal naris
that is suspended between the posteromedial processes
of the hyoid (Fig. 4-3). The larynx separates the conflu- Vornerine teeth
ence of the lungs from the buccal cavity at the level of Entry to esophagus
the esophagus. Viewed from the buccal cavity (Fig. 4-4), Eye bulge
the superior or pharyngeal aspect of the larynx is marked Eustachian tube
by a vertical opening, the glottis, through which air moves
Jaw muscles
between the mouth and lungs.
(cut)
Movement of the arytcnoid cartílagos is affected by
three (four according to some authors) pairs of muscles Glottis
associated with the pharyngeal surfaces of the cartílagos Vocal sac
(Fig. 4-3). The m. dilatator laryngis originales lateral to aperture
the arytenoid from the posteromedial process of the hyoid Floor of mouth
and inserís near the apex of the cartilage adjacent to the Tongue
glottis. Contractíon of this muscle pivots the arytenoid
cartilage in the cricoid ring in such a way that the pha-
ryngeal margin of the valve is deflected laterally and the Lower jaw
cardiac margin is moved medially, thereby stretching and
increasing the tensión of the vocal cord located inside the Flgnre 4-4. Generalized anuran buccal cavity showing principal
structures.
cartilage. The two remaining pairs of muscles are con-
strictors. The m. constrictor laryngis externus of W. Mar-
tin and Gans (1972) and Trewavas (1933) lies adjacent nate from the hyoid. Rather than inserting on the ary-
to the anteroventral margins of the arytenoids; this is the tenoid cartílages, members of each pair of muscles insert
m. hyolaryngeus of Schneider (1977) and the m. sphinc- on one another. Thus, when these constrictors contract,
ter anterior of Gaupp (1904). The m. constrictor laryngis they slide anteriorly over the arytenoid cartílages, pushing
anterior of W. Martin and Gans (1972) lies adjacent to the two structures together (Gans, 1973b).
the posteroventral margins of the arytenoids; this is the Although the cricoid cartilage, together with its processes,
m. sphincter posterior of Gaupp (1904), mm. sphincter has extremely variable structure among anurans (see
anterior + sphincter posterior of Schneider (1977), and Ridewood, 1887, 1900; Trewavas, 1933), certain struc-
mm. constrictor laryngis anterior + constrictor laryngis tural characteristícs are critical to its role in suspensión
posterior of Trewavas (1933). Both sets of muscles origi- and support of the laryngeal system. The cricoid ring
 Vocalization
forms a firm base against which the aiytenoid carülages coid and thyrohyal cartilages are greatly enlarged and 91
can be pivoted. In most anurans having a complete ring modified into an ossified (or partly ossified) box which
and vocal cords, the posterior (cardiac) end of each cord parüally endoses modified arytenoid elements. Vocal cords
É attached to the inner margin of the cricoid cartilage, as are absent, but in Pipa the cricoid chamber contains two
well as the posterior margin of the arytenoid cartilage. As bony rods that termínate and articúlate with one another
the arytenoid cartilage is pivoted, the vocal cord is anteriorly via carülaginous discs (presumably represent-
stretched; the resultant tensión is increased by the partial ing modified arytenoid cartilages). Each disc bears a ten-
altachment of the vocal cord to the relatively rigid cricoid dinous connection to a large muscle originatíng from the
ring. The esophageal and bronchial processes (Fig. 4-3) base and covering the exterior side of the laryngeal
oí the cricoid cartilage support the proximal confluence chamber (Fig. 4-6). G. Rabb (1960) hypothesized that
oí the lungs. The chamber thus defined is termed the movements of either one of these two muscles caused
posterior, or lower, laryngeal chamber (Fig. 4-5) and is the joint to open. In the course of opening, the cartila-
overlain by the arytenoid cartilage complex. When present, ginous disc slips or pops anteriorly, and so produces the
the esophageal process is located at the midline on the sharp, metallic clicking noise that characterizes vocaliza-
posterior margin of the cricoid ring; thus, the process tion in these frogs. A similar mechanism is known in Xen-
overlies and marks the confluence of the right and left opus borealis (Yager, 1982). Unlike other anurans, pipids
lungs. One bronchial process arises- from each side of the are distinguished by the presence of bronchial tubes lead-
cricoid ring and curves posteroventrally beneath the an- ing to posteriorly positioned lungs; the bronchial processes
terior terminus of the right and left lung, respectively, so of the cricoid cartilage and the posterolateral processes
as to support their unión as the posterior laryngeal cham- of the hyoid píate are modified for support of the bron-
ber. The term "bronchial process" is misleading. With chial tubes.
the exception of some pipids, the lungs of anurans arise
cfirectly from the posterior laryngeal chamber; bronchial
and tracheal tubes (associated with the development of
a neck región) are absent. The cricoid cartilage bears one -Esophageal process
remaining pair of processes: the articular processes that M. sphincter anterior
arise laterally from the cricoid ring and provide a pivotal Posterior
point of articulation between the cricoid-laryngeal assem- membrane ¡(Vl.dilatator laryngis
blage and the hyoid apparatus via the bony, postero- Fibrous mass-
|\ryteno¡d cartilage
medial processes of the hyoid píate. Vocal cord
A cross-sectional view of the laryngeal complex (Fig. Posterior M. hyolaryngeus
chamber
4-5) ¡Ilústrales the relationship of the ventral, or posterior,
Bronchial
chamber to the dorsal, or anterior, chamber composed process Cricoid cartilage
of the arytenoid cartilages and their associated structures.
The two chambers are separated by a pair of mem- Figure 4-5. Isometric cross-sectional view of an anural laryngeal
apparatus. Adapted from W. Martin (1972).
branes, each of which is formed by a medial extensión
of the lining of one of the arytenoid cartilages. These
membranes are thought to direct air over the vocal cords,
Isthmus of hyoid píate
which lie just above them. As mentioned previously, one
vocal cord is associated with each arytenoid cartilage; the Arytenoid cartilage
anteroventral (pharyngeal) terminus attaches to the inner
Articular surface
end of the arytenoid cartilage, whereas the p'osterodorsal Cricoid cartilage of rod with roof
(cardiac) end usually is connected to both the arytenoid of larynx
and cricoid cartilages. The vocal cords are derived from Dilatator
the lining of the arytenoid cartilages and, therefore, are muscle Arytenoid rod
membranous in origin; however, their configuration is
extremely variable among species. Differences include
the extent and nature of the attachments between the
vocal cord and the arytenoid cartilage and the size and
shape of the fibrous masses that may be associated with
the cord. These structural variations modify the way in Cricoid cartilage
which the vocal cords víbrate. This factor, in combination
with the size of the organism and the shape and mass of
the arytenoid cartilages, determines the fundamental fre-
Bronchial tube
quency of sound produced by the frogs.
The pipids are sufficiently divergent to warrant special Figure 4-6. Diagram of laryngeal apparatus of Pipa pipa. Adapted
comment. In members of this tongueless group, the cri- from Ridewood (1897) and G. Rabb (1960).
LIFE HISTORY
92

Figure 4-7. Inflatecl externa)

subgular vocal sac of the Mexican
toad, Bufo marmóreas. Photo by
W. E. Duellman.

Vocal Sac (1935b) scheme of classificatíon, there are three basic

Although both male and female frogs possess functíonal kinds of muscular vocal sacs: median subgular, paired
laryngeal apparatuses, the structures are better devel- subgular, and paired lateral. The most generalized and
oped in males (i.e., they are larger relative to body size widespread of these is the median subgular sac, which is
and have more robust musculature). Moreover, only males a single sac in the throat. Derived conditions are repre-
possess vocal sacs, which have been considered primarily sented by paired subgular sacs (which are completely or
as resonaüng chambers for sound productíon but may incompletely separated from one another) and paired
funcüon in some species at least as sound-couplers or lateral vocal sacs that are morphologically discrete struc-
acoustic radiators to the air around them (Watkins et al., tures located posteroventral to the angle of the jaw on
1970). Acoustic energy that is transduced by the laryn- either side of the head. All three types of vocal sacs may
geal apparatus acts on the buccal cavity and vocal sac. be categorized as being "internal" or "external." Internal
The vibration of these structures intensifies the acoustic sacs are characteristíc of, but not restricted to, frogs that
signal, resonaüng and radiaüng it across the surface of cali from water (Fig. 4-8). Because of their effect on
the vocal sac into the air. A few male frogs that vocalize buoyancy, large external vocal sacs would be disadvan-
do not have vocal sacs. tageous under water. Calis of frogs having infernal vocal
In representatíves of some primitive groups (e.g., dis- sacs, like those in which the sacs are absent, have low
coglossids and myobatrachids), the lining of the mouth frequencies, presumably because of the small degree of
is loóse and folded on either side of the tongue to form flexibility of the resonatíng chamber (Littlejohn, 1977).
a pocket. When the buccal cavity is filled with air, the According to Noble (1931b), if the sacs are internal, the
pocket is distended; Liu (1935b) viewed this as a prim- skin covering them is unmodifled; when the sac is in-
itive form of vocal sac. Among the majority of anurans flated, the área assumes a "swollen" appearance. In con-
that possess well-developed vocal sacs, the sac is formed trast, the presence of an "external" vocal sac is indicated
as a diverüculum of the lining of the buccal cavity. The by modifications of the overlying skin that include: (1)
diverüculum lies between the superficial mandibular the presence of discrete, inverted or everted dermal lobes
muscles (m. intermandibularis and m. interhyoideus of to receive the underlying muscle when the sac is inflated;
Tyler, 1971a) and the deeper geniohyoideal musculature (2) extensivo, irregular pleatíng or folding of the skin over
of the lower jaw. The sac communicates with the buccal the entíre submandibular región; or (3) the presence of
cavity via paired, round or slitlike valves (vocal slits) in single pre- or postaxillary folds (Üu, 1935b; Tyler, 1971a).
the floor of the mouth; the valve lies between the m. An esoteric modification of the paired subgular vocal sac
geniohyoideus medially and the mandible laterally. Vari- occurs in African ranids of the genus Ftychadena. In these
ous myointegumental attachments determine the posi- frogs, there are paired, submandibular guiar slits (i.e.,
tíon of the inflated sac (Tyler, 1971b). Following Liu's obliquely oriented invaginations of guiar skin; not to be
 Vocalization
93

Figure 4-8. Inflated interna! lateral

vocal sacs of the Mexican burrowing
frog, Rhinophrynus dorsatis, which
calis from the surface of water. Photo
by W. E. Duellman.

Nostril (open) the lungs at two stages (interspersed among sepárate os-
Buccal cavity cillatory cycles)—from outside to the buccal cavity prior
Tongue Larynx (open) to exhalaüon of pulmonary air through the larynx, and
from buccal cavity to the lungs after exhalation (Figs. 4-
9, 4-10). An inflation cycle involves a gradual increase
followed by a decrease of inflated lung volume and pres-
sure achieved throughout a series of ventílatory cycles.
These ventílatory cycles are powered by muscle activity
in the floor of the buccal cavity; some of their energy is
stored in the elastíc fibers and smooth muscle of the lung
Vocal sac (i.e., pulmonary pressure). Pulmonary energy stores are
aperture released when air is expulsed from the lung. At the end
of the inflation cycle, the muscular body walls, which
Figure 4-9. Schematic representaron of an anuran showing those have become distended to accommodate increased lung
structures involved ¡n vocalization.
size, contrae!; this results in the forced expulsión of air
from the lungs and the consequent reléase of pulmonary
confused with vocal slits) through which the vocal sac is energy stores.
everted when it is inflated (Inger, 1956a; K. Schmidt and On the basis of electromyographic evidence, W. Martín
Inger, 1959). and Gans (1972) confirmed that during vocalizatíon the
arytenoid cartílages sepárate to open the glottís in re-
Sound Production sponse to pulmonary pressure raised by contraction to
In producing sound, the anuran larynx is the transducer the body wall rather than by direct activity of the dila-
that converts muscular acüvity into acoustic energy through tators. Prior to vocalizing, the frog uses the dilatators in
the manipulation of air flow by the force-pump mecha- combination with the constrictors to retract the laryngeal
nism. The patterns of air flow involved in anuran respi- apparatus ventrally between the posteromedial processes
ratory cycles and the muscular activity responsible for of the hyoid; in this positíon the arytenoid cartílages are
them were described in detail by de Jongh and Gans locked together. In most anurans the onset of vocalizatíon
(1969); W. Martín and Gans (1972) subsequently ex- is marked by (1) the culmination of the contraction of
plained the relatíonship between air-flow patterns and the body wall, and (2) the abrupt relaxatíon of the lar-
vocalization in the toad Bufo valliceps. Oscillatory cycles yngeal dilatators and constrictors. The first event induces
of respiration involve the exchange of atmospheric air an air pressure behind the larynx that overcomes the
with that in the buccal cavity via the nostrils. In the more relaxing muscles, thereby shifting the laryngeal apparatus
complex ventílatory cycle, atmospheric air is pumped into anterodorsally and bursting open. Both the constrictors
LIFE HISTORY
94

Larynx opens

Sternohyoid muscle
contraéis

Buccal floor
muscles relax

Buccal floor
muscles contrae!
Nares cióse and
1A
buccal floor muscles
contract

Body wall contracts;

vocal sac aperture opens Vocal sac aperture
and sacs are inflated closes and air
shifted back
Buccal floor
muscles contract

2D
,V

Nares open.
larynx closes,
and
buccal floor muscles relax
Figure 4-10. Graphic representation of anuran vocalization with résped to airflow. Peripheral figures
(1A-2D) depict the ventilation cycle, and 1A and IB show the oscillatory cycle. Vocalization is represented
in Figure 4-9 as an alternative state to 2C. Major strudures involved are labeled in Figure 4-9. Broken
arrows show diredion of air movement. Solid arrows associated with lungs and guiar región indícate
effective forcé of applied muscle adivity, whereas open arrows represent movement of floor of mouth
resulting from adion of gravity combined with relaxation of muscles. Modified froni Gans (1973b).

and dilatators are effectively inactive during sound pro- ration rather than expiration (Zweifel, 1959; Lórcher,
duction. Thus, as pulmonary air rushes over the vocal 1969).
cords and arytenoid cartilages, thesc structures víbrate.
They produce a sound, the frequency of which varíes Sound Reception
interspecifically depending in part on the tensión of the Anurans have a unique and complex receptor and pe-
vocal cords and effective mass of the arytenoid cartilages. ripheral nervous system for selective processing of acous-
These physical parameters are controlled by a pair of tic signáis. In most species, the primary sound receptors
dilatator muscles. The resonating sound in the buccal are the external ears, but the forelimbs also function in
cavity and vocal sac (if present and inflated) is transmitted phonoreception (Hetherington and Lombard, 1982). Here
across the surface of the vocal sac(s). However, Bambino the concern is how these structures function in hearing
bombina and B. variegata produce their calis on inspi- (for the details of structure, see Chapters 2 and 3). Most
 Vocalization
anurans possess a large tympanic membrane of thin, movements of the tectorial membranes. The exact acous- 95
aonglandular skin. This extemal ear is the receptor of tic pathways in the fluids are unknown. Possibly the dis-
afcbome sound waves and transfers sound pressure into turbance is channeled through perilymphatic pathways,
Jbrations of the columella in the middle ear. These vi- across the thin membranes, and trien to the endolym-
taaóons, in turn, disturb the fluids in the inner ear at the phatic fluid around each of the auditory organs (Wever,
jBKrface, that is, the oval window, of the columella and 1973). Alternatively, the disturbance may be in a straight
ase inner ear. The tympanic membrane is much larger path to the organs, thus implying that the membranes
ten the oval window, and this difference in size is sig- separating the perilymphatic and endolymphatic spaces
«ficant in matching the acoustic impedance of air to the provide no selectíve transmission route (Capranica, 1976).
ügher impedance of the fluids in the inner ear; in this In addition, the fluid pathways may be frequency-de-
way sensitivity to airborne sounds is maximized (Capran- pendent, thereby affording selection of different frequen-
ra. 1976). cies to the two organs (Lombard and Straughan, 1974).
The oval window, the sensory opening to the inner Various studies on acoustic reception have provided
ear. is abutted laterally not only by the footplate of the information on the funcüon of the middle and inner ears
oolumella but also by the operculum. Each of mese mid- of frogs. Capranica (1965) and Loftus-Hills and John-
de-ear bones has a muscular attachment to the ventral stone (1969) demonstrated that frequencies below 1000
sjrface of the suprascapula. Contraction of the m. op- Hz are processed by the papilla amphibiorum and that
«cularis and relaxation of the m. columellaris leave the higher frequencies are received by the papilla basilaris.
enkimella free to víbrate at the oval window, whereas the Lombard and Straughan (1974) showed that the oper-
reverse contractíon and relaxation tends to immobilize cular complex conducís airborne acoustic signáis at fre-
fie columella and reduce transmission to the inner ear quencies below 1000 Hz and that the tympanic-colu-
fWever, 1979). This interlocking mechanism provides frogs mellar complex transduces signáis at higher frequencies.
*tih great control of acoustic reception, and (1) presum- These conclusions were supported by Chung et al. (1978),
abíy functions to protect the receptors of the inner ear who calculated that reception of sounds at frequencies
frotn overstimulation, and (2) possibly functions to select above 1000 Hz by somatosensory and vestibular systems
for reception of vibraüons from different acoustic path- is ineffective, and concluded that the peripheral auditory
•ays, via the columella or the opercular complex. apparatus in anurans is adapted for the detection of fre-
Within the inner ear there are two sepárate auditory quencies above 1000 Hz. Thus, the tympanic-columellar
ofgans (papilla amphibiorum and papilla basilaris) that complex in the middle ear and the papilla basilaris in the
jeceive sümulation through the disturbance of the fluids inner ear, a combination of structures present in totality
in the middle ear. Each of the papillae organs possesses only in anurans, constitute the primary receiving system
hair cells and a sepárate tectorial membrane. Motion in for adverüsement calis (Fig. 4-11). Different degrees of
tte perilymphatic fluid caused by vibraüon of the oval acoustic selectivity in the inner ear have been demon-
window is coupled with the endolymph, which causes strated in various frogs. The ear of the bullfrog Rana

External i
Ear H

01,000 Hz

Tympanum

Figure 4-11. Diagram of an anuran

auditory system. Solid arroyvs
indícate transmission pathway of
frequencies of less than 1000 Hz via
the opercular papilla amphibiorum
M. opercularis complex; open arrows indícate
transmission pathway of frequencies
of more than 1000 Hz via the
tympanic-columellar-papilla
< 1,000 Hz basilaris complex.
LIFE HISTORY
catesbeiana selects species-specific properties of the ad- experience, the peripheral auditory system of anurans is
vertisement cali (Capranica, 1965). In the cricket frog, likely to be more static. To change the sensitivity of a
Acris crepitans, frequency response also is geographically sensory receptor, partícularly the ear, which is a me-
specific (Capranica et al., 1973). In Eleutherodacfylus chanical organ, would seem to require a very gradual
caqui there is sexual discrimination of the two notes at evolutionary process. The inadvertent introduction of a
different frequencies in the compound advertisement cali foreign species or a rapid change in the sonic and breed-
(Narins and Capranica, 1976); sexual differences exist in ing environment could be disruptive."
the sharpness of tuning and the frequency of máximum Because temperature affects both the sound-producing
sensiüvity of the papilla basilaris (Narins and Capranica, mechanisms and the acoustic signáis, it is only reasonable
1980). to expect that the sensitivity of the auditory receptors is
Loftus-Hills (1973) suggested that the characterisücs of temperature-dependent. Mohneke and H. Schneider
the tympanic membrane (probably its área primarily) are (1979) and Hudl and H. Schneider (1979) obtained au-
the principal factors influencing auditory sensiüvity in diograms from the torus semicircularis of four European
anurans, but Frishkopf et al. (1968) found no correlatíon species of frogs at four temperatures; latencies became
between tympanum size and auditory sensitivity among shorter with increased temperature and higher frequen-
juveniles and adults of Rana catesbeiana, in which tym- cies. The auditory receptors of three of the species func-
panum size is much different in males and females. tioned well at 5°C, but at that temperature the receptors
Chung et al. (1978) and Pettigrew et al. (1978) dem- of Bombina uariegata were rather insensitive. Tempera-
onstrated that the buccal cavity, to which the middle ears ture effects are most pronounced at frequencies below
are connected via the Eustachian tubes, functions as a 1000 Hz; thus, it seems as though temperature affects
resonator. Pressure generated by the displacement of one the opercularis-papilla amphibiorum pathway more than
tympanum is transmitted through the buccal cavity to the the tympanic-columellar-papilla basilaris pathway.
other tympanum, thereby reducing its net vibration. This
tympanic coupling results in differenüal sound-pressure Central Control Mechanisms for
levéis and enhances the ability to determine the direction Sound Reception and Vocalization
of the source of the sound. Results of experiments on The papilla basilaris and papilla amphibiorum are inner-
phonotaxis in the tree frog, Hyla cinérea, support the idea vated by discrete fibers of Cranial Nerve VIII (auditory);
of differenüal sound-pressure levéis in localization of these fibers maintain their integrity as they enter the med-
acoustic sources in frogs (Rheinlaender et al., 1979). ulla oblongata and continué anteriad to the torus semi-
The auditory role of the opercular complex and papilla circularis, the major receiving site for auditory fibers be-
amphibiorum responsible for the transmission and per- low the optic ventricle of the midbrain. In most species
cepüon of low frequencies (Fig. 4-11) apparently is the of frogs examined, the auditory nerve contains three types
same in anurans and salamanders, but the precise ex- of fibers, each having distinct excitatory frequencies; an
ternal receptors of sound waves are questionable. The exception is Scophiopus couchii, which lacks fibers car-
presence of this system is correlated with terrestrial habits; rying intermedíate frequencies (Capranica, 1976). The
premetamorphic amphibians and adults of some aquaüc low- and mid-frequency fibers innervate the papilla am-
salamanders and frogs (leiopelmatíds and pipids) lack the phibiorum, and the high-frequency fibers innervate the
opercular complex. papilla basilaris. Pettigrew et al. (1978) demonstrated that
In some fossorial anurans and others that live in and discrete áreas of neural tissue in an anterior-posterior axis
along streams, the tympanic-columellar system is re- of the torus semicircularis act as receptors; each receptor
duced or lost. Reducüon begins peripherally and pro- área is broadly tuned to a different frequency range and
ceeds medially, so that the sequenüal loss is tympanum, to sound from different directions. This "map" of audi-
extracolumella, distal part of columella, and flnally prox- tory space in the midbrain is comparable to the visual-
imal part of columella. Insofar as is known, in no frog perceptual field on the tectal surface; one side of the brain
have both systems in the middle ear been reduced or attends to contralateral auditory space. According to Pet-
lost. Both the papilla amphibiorum and basilaris are present tigrew et al. (1978), "The inner ear and the midbrain
in Bu/o bocourti and Ascaphus truel, which lack colu- [each] are performing a sepárate Fourier analysis of the
mellae and tympana (R. Schmidt, 1970). sound. With the low and intermedíate frequency com-
The unique auditory complex in anurans having two ponents, the animal can determine on which side its mat-
receptor systems (also two in crickets) allows for the in- ing partners are located; once the animal orients towards
acüvaüon of the low-frequency system, thereby en- the source of the sound, it can then utilize the high-fre-
hancing the ability to perceive specific informatíon in ad- quency components of the mating cali for guidance."
vertisement and territorial calis. The emphasis on peripheral Furthermore, it has been shown that Rana pipiens has a
hearing is important in specific acoustíc recognition. But class of neurons in the central auditory system that re-
there are evolutíonary constraints, as noted by Capranica sponds selectively to particular rates of amplitude mod-
(1977): "While the central nervous system of higher ver- ulation (G. Rose and Capranica, 1983).
tebrates may be 'plástic' and readily alterable through Stimuli to initiate vocalizations may be hormonal,
 Vocalization
Androgen Receptors 97
(Área of ventral magnocellular preoptic nucleus)

Acoustic Receptors
(Papilla basilaris +
papilla amphibiorum) Forebrain bundles

Nerve VIII
I
AFFERENT VOCAL CENTER
(Área of main sensory nucleus V)

Lung Stretch
Receptors?
Spino- + bulbo- Direct + crossed tegmento-bulbar tracts
tegmental tracts

Pain & Touch

Receptors
I
EFFERENT VOCAL CENTER
(Área of vagal + hypoglossal nuclei)

I
Respiratory-Vocal Muscles
Wl^rntí 4-12. Model of the neurological basis of vocalization mechanisms in anurans. Modified from
B. Schmidt (1971).

acoustic, or tactile (R. Schmidt, 1973). Testícular devel- are initiated by stimulation of the skin of the trunk (Dia-
opment is dependent on gonadotropic hormones pro- kow, 1977); an internal afferent source inhibits the re-
duced by the pituitary; activated interstitial tissue in the léase cali.
lestes produces androgenic hormones. The androgen re-
ceptors in the ventral magnocellular preoptic nucleus in
the midbrain actívate a hypothesized afferent vocal center KINDS OF VOCALIZATIONS
(R Schmidt, 1971). This center may receive a variety of AND THEIR FUNCTIONS
sensory inputs; these are analyzed, and the appropriate The following classification of anuran vocalizations is based
vocal response, if any, is transmitted posteriorly to an on that by Bogert (1960), as modified by Littlejohn (1977)
efferent vocal center, which generales patterns of calling and Wells (1977b), and emphasizes the functional as-
movements (Fig. 4-12). Audioradiographic studies of the pects of the calis.
pipid Xenopus laevis indícate that androgens (dihydro-
testosterone and estradiol) are concentrated in the torus 1. Advertisement cali. Formerly known as the
sernicircularis (D. B. Kelly, 1980). Appropriate tactile in- mating or breeding cali, it is emitted by males
put into the afferent vocal center elicits reléase calling. and has two functions: (1) attraction of con-
The basic neurological system for vocalization apparently specific females, and (2) announcement of
is present in both sexes. R. Schmidt (1966) implanted occupied territory to other males of the same
testes and anterior pituitary glands of Rana in the body or different species. In some species the ad-
cavities of female tree frogs, Hyla cinérea, and induced vertisement cali conveys only one set of in-
them to produce advertisement calis in response to taped formation (courtship or territorial), but in other
calis of that species. D. B. Kelly (1980) suggested that species a compound advertisement cali con-
hormonal concentration by laryngeal motor neurons in- veys both sets of information. Three kinds of
dicates that androgens regúlate the final common path advertisement calis are recognized:
for vocal behavior and that modulation of auditory sen- A. Courtship cali. Produced by males in an
sitivity by hormones could explain seasonal variations in attempt to attract conspecific females.
behavioral responses to conspecific vocalizations. B. Territorial cali. Produced by a resident male
Reléase calis by unreceptive females of Rana pipiens in response to an advertisement cali re-
LIFE HISTORY
98 ceived above a critical threshold of inten- corporal vibrations produced by a male or an
sity. unreceptíve female in response to amplexus.
C. Encounter cali. Evoked during close-range 4. Distress cali. A loud vocalization produced by
agonisüc interactions between males. either sex, usually with the mouth open, in
2. Reciprocation cali. Given by a receptíve female response to disturbance.
in some species in response to advertisernent
calis of conspecific males. Advertisement Calis
3. Reléase cali. An acousüc signal associatcd with These are the primary vocalizations in anurans. Early ex-

6-

4-

2-

2-

° 4H

2-

O
D
4-

2-

4-

2-
Figure 4-13. Anuran advertisement
calis. A. Pipa carvalhoí (courtesy of
Peter Weygoldt). B. Rhinophrynus
dorsalis. C. Gastrophryne olivácea.
D. Dendrobatos pumilio. E. Bufo 0.2 0.4 0.6
valliceps. All are narrow-band
(45-Hz) displays. Time in Seconds
 Vocalizar^
periments on hylid frogs of the genus Pseudacris by Mar- acousüc signáis by the bullfrog Rana catesbeiana. Loftus- 99
lof and Thompson (1958) and Littlejohn and Michaud HUls and Littlejohn (1971b) and Straughan (1975) showed
11959) showed that females responded posiüvely to ad- that pulse repetitíon rate was the only component of the
vertsement calis of their own species but were indifferent calis used for discriminaüon by two sympatric pairs of
to calis of other species. Subsequent neurophysiological hylid frogs—respectively, Litaría ewingii and L. uenreauxii
studies helped to isolate those components of the acous- in southeastem Australia and Hyta cadaverina and H.
•c signáis evoking responses by females. For example, regula in California. In contrast, females of H. cinérea
Capranica (1965) demonstrated different responses to respond only to bimodal frequency components of the

4-

4-

2-

t f I,

w ,'áw

IP- ir Figure 4-14. Anuran advertisement

2- calis. A. Leptodactylus
pentadactylus. B. Olotygon
bou/engerí. C. Centrolenella
grandlsonae. D. Physalaemus
pustulosas. E. Eleutherodactylus
0.2 0.4 0.6 caqui (courtesy of Peter M. Narins).
F. Hyla bokermanni. All are narrow-
Time ¡n Seconds band (45-Hz) displays.
LIFE HISTORY
100 advertisement cali (H. Gerhardt, 1974b). In the neotrop- produced rapidly, so as to result in a trill (Fig. 4-13). The
ical leptodactylid, Physahemus pustuhsus, females se- same is true in Xenopus (Vigny, 1979), in which two
lectively choose larger males by distinguishing lower fun- species (X. íaeuis and X. ruwenzoriensis) have harmonics
damental frequencies in the courtship cali (M. Ryan, reaching ultrasonic levéis—80 and 150 kilohertz, respec-
1980a). tively. In many species the cali consists of two or more
The determination of species-specific cali discrimina- notes, or groups of notes, having different acoustic prop-
tion by females led to the study of the advertisement cali erties (Fig. 4-14). Such calis are common among some
as a premating isolating mechanism in North American groups of hylids (Duellman, 1970); leptodactylids, espe-
toads (W. Blair, 1956), Australian myobatrachids of the cially Eleutherodactylus in the West Indies (Drewry, 1970);
genus Crinia (Littlejohn, 1959; Littlejohn and Watson, some species of Rana (Mecham, 1971); and some Aus-
1974), and Central American hylid frogs (Fouquette, 1960; tralian myobatrachids (Pengilley, 1971; A. Martin et al.,
Duellman, 1967b). These and many other such studies 1980).
have confirmed the species-specific acoustic properties in The Puerto Rican frog Eleutherodactylus caqui has a
a diversity of anurans. biphasic compound cali (Fig. 4-14E); the first note, "co,"
Some notable cases of geographic variation in adver- evokes responses from males, whereas the second note,
tisement calis have been discovered in North American "qui," evokes responses from females (Narins and Ca-
cricket frogs, Acrís (Nevo, 1969); Central American hylid pranica, 1976, 1978). The aquatic South American Pipa
frogs (Duellman, 1970); neotropical poison-dart frogs, carvalhoi produces an advertisement cali consisüng of a
Dendrobates (Myers and Daly, 1976); and toads, Bu/o series of clicks (Fig. 4-13A), usually followed by a long
uiridis, in Europe and southwestern Asia (Nevo and buzz (Weygoldt, 1976a).
Schneider, 1976). Detailed studies of geographic varia- In the Central American Hyla ebraccata the buzz-like
tion in advertisement calis have been completed on Hyla primary note evokes agonistic replies from other males,
regula (W. Snyder and Jameson, 1965), Acris (Capranica whereas the series of shorter click-like notes are produced
et al., 1973), andH. arbórea (Schneider, 1977). when the frogs are in a breeding chorus (Wells and Greer,
The genetic basis for the advertisement cali is indicated 1981). Similar responses to an initial, long note received
by the production of distinctive calis by interspecific hy- at an intensity of more than 100 dB by males of the
brids. The presence of an intermedíate cali in a hybrid Australian Geocrinia Victoriano result in the production
population of the hylid frogs Hyla cinérea X H. gratiosa of a territorial note and subsequent agonistic behavior
in Alabama was first documented by Mecham (1960); (Littlejohn and P. Harrison, 1981). Likewise, males of
this was verified in hybrids between the same species in the Australian Uperoleia rugosa switch from advertise-
Georgia (H. Gerhardt et al., 1980). Natural hybrids be- ment calis to a territorial cali and attack males that intrude
tween the spadefoot toads, Scaphiopus bombifrons and into a territory (Robertson, 1981). The same behavior
S. hammondii, have cali components intermedíate be- has been observed in the South African Phrynomerus
tween those of the parental species (Forester, 1973). There annectens, in which both resident and intruder produce
are disünct differences in pulse rates between natural hy- aggressive calis prior to wrestiing in water (Channing,
brids and parental toads Bu/o americanus and B. wood- 1976).' South African species of the ranid genus Pty-
housü fowleri (Zweifel, 1968). The calis of the natural chadena have advertisement calis made up of long, pulsed
hybrids between the Australian myobatrachids Geocrinia notes; in dense choruses the notes are shortened, and
laevis and G. Victoriano contain components of both pa- these aggressive calis have greatly increased pulse rates
rental species and evoke positive responses from females (Passmore, 1977). The dendrobatid Co/osiethus inguin-
of both species (Littlejohn and Watson, 1976). Among alis has an advertisement cali consisting of a long series
natural hybrids of three pairs of sympatric species of North of short peeps; territorial intrusions result in an encounter
American hylid frogs, the calis of hybrids between Hyla cali consisting of a long peep followed or not by a shorter
auiuoca and H. chrysoscelis, and between H. graíiosa note (Wells, 1980a). In this species both males and fe-
and H. cinérea, are intermedíate between the calis of the males also emit a close-range encounter cali consisting
parental species, whereas the calis of the hybrids between of a low-intensity chirp. Three kinds of calis—advertise-
H. femoralis and H. chrysoscelis are more like the cali of ment and two kinds of encounter calis—are produced by
the latter; in two-way discrimination tests, females of H. the bufonid Atelopus chiriquiensis (Jaslow, 1979). The
chrysosce/is, femoralis, and graíiosa discriminated against North American tree frog, Hyla cinérea, emite territorial
the appropriate hybrid and females of H. cinérea showed calis at dusk, followed by a period of movement to ponds,
parüal discrimination (H. Gerhardt, 1974a). during which time aggressive calis are produced; once
Despite the limited vocal repertoire of anurans, there males are situated at calling sites at ponds, courtship calis
is much variation among species in the nature of the are emitted (Cartón and Brandon, 1975).
advertisement calis. In many species the advertisement In the leptodactylid Physalaemus pustulosus, which can
cali consists of a single note; in others the cali is made emit acoustically different courtship and aggressive notes
up of a series of identical notes. In most toads of the simultaneously (Drewry et al., 1982), cali complexity in-
genus Bu/o and some other anurans, identical pulses are creases as the number of males in a chorus increases and
 Vocaharon
in responsc to (1) playbacks of a background chorus, (2) ent calis for advertisement and territorial encounters
playbacks of more complex calis, (3) increased cali in- (Wiewandt, 1969; Wells, 1978b). Such calis are pro-
tensity by nearby males, and (4) approach of other frogs duced at times of close-range encounters and usually
into the visual field of the calling male (Rand and M. consist of signáis with different durations or pulse rates
Ryan, 1982). These are but some of the ways of increas- than the advertisement calis. Agonistic signáis are size-
ing the information contení of the advertisement cali in related in R. clamitans; calis of small males elicit strong
response to calis of other males. Other ways of increasing agonistic vocalizations from small adult males, whereas
the information content include (1) lengthening the cali, calis of large males elicit agonistic responses from large
(2) increasing the note repetition rate, (3) adding notes males and weak responses from small males (Ramer et
to the cali, and (4) adding new kinds of notes (Wells, al., 1983). Encounter calis probably are much more com-
1977b). Similar modifications can be hypothesized for mon than suggested by the few documented observa-
the evolutíon of compound advertisement calis from sim- tions by McDiarmid and Adler (1974), Weygoldt (1976a,)
ple calis (Fig. 4-15). Wells (1977a), and Jaslow (1979). In many cases en-
Upon the approach of females, some frogs are known counter calis are associated with postural or other visual
to change the properties of their advertisement calis. In displays and precede physical combat between males.
the dendrobatid Colostethus collaris, calis lasting 10-20 Territorial calis function as spacing mechanisms among
seconds are normally produced only once every several males and are most common among species that have
minutes, but when a female approaches to within 10-15 prolonged breeding seasons. In large concentraüons of
cm of the male, the interval between calis is reduced to conspecific, explosive breeders, such as some pelobaüds
about 5 seconds (Dole and Durant, 1974b). A similar (Scaphiopus) and many toads (Bufo) among others, de-
modification prevails in Colostethus Mnitatus, which also fense of territories is not favored; however, some explo-
ulereases the number of notes per cali group (Wells, sive breeders (e.g., African ranids, Ptychadena) have ag-
1980b). Centrolenella fleíschmanni intersperses soft mews gressive calis (Passmore, 1977). On the other hand, what
amidst normal long-range courtship peeps when a female has been described as the mating calis of many species—
approaches (Creer and Wells, 1980). In the nest-building especially tropical frogs that do not congrégate for breed-
gladiator frog, Hyla rosenbergi, the advertisement cali ing (e.g., Eleutherodactylus)— actually may be com-
changes to a slower, softer courtship cali when a female pound advertisement calis or solely territorial calis.
enters a nest in which a male is calling (Kluge, 1981). Advertisement calis are involved in other intraspecific
Territorial calis containing agonistic signáis may be in- social interactions among males of many species (Wells,
corporated into a compound advertisement cali, such as 1977a). Duellman (1967a) suggested different kinds of
in Eleutherodactylus coqui, Physalaemus pustulosus, and organization of choruses into duets, trios, or quartets.
presumably Hyla bokermanni (Fig. 4-14), or produced Like many hylids, there is synchronization of vocal activ-
independently from the advertisement cali. Playbacks of ity in the European tree frog, Hyla meridionalis, but the
conspecific advertisement trills and the mating trill of Bufo chorus structure changes from duets and trios when few
ualliceps evoked territorial chuckle-calls from males of the males are calling to no organization when many males
sympatric Rana beriandieri (Gambs and Littiejohn, 1979). are calling (Paillete, 1976). Alternation and synchrony of
The Pacific tree frog, H. regula, produces a diphasic ad- calling is best developed in species with prolonged breed-
vertisement cali, but the approach of a female or a silent ing seasons and regularly spaced, repetitive calis (Wells,
male results in a monophasic cali (Whitney, 1981). An- 1977a). Advertisement calis might be separated tempo-
other tree frog, H. crutífer, has an advertisement cali rarily so as to minimize acoustic interference and thereby
consisting of a single note, but a trill is emitted when maximize an individual male's chances of attracting a
another male is cióse by (M. Rosen and Fellers, 1974). mate (Littiejohn and Martin, 1969; M. Rosen and Fellers,
Rana clamitans and R. catesbeiana have disünctly differ- 1974). Loftus-Hills (1974) suggested that anurans have

Simple Advertisement

Territorial
f
| Cióse Range
Courtship
Encounterllllll Figure 4-15. Hypothetical modifications of a
simple advertisement cali in the evolution of a
compound advertisement cali and an encounter
cali. Lines and squares represent different kinds
of notes derived from an original common type
and recombined into a complex advertisement
Compound Advertisement cali. Modified from Wells (1977b).
LIFE HISTORY
102
Figure 4-16. Diagrammatic representation of
calling sequences of eight individuáis of the
hylid frog Smilisca baudinii (blocks 1-8). The
leading edge of the plañe represents time, and
the lateral edge represents social organizaton
into duets (A-D). Redrawn from Duellman
(1967a).

a ncural pacemaker but that the basic calling rate of each include frogs in their diets, and Tuttle and M. Ryan (1981)
individual can be altered by interactions with other calling experimentally demonstrated that the Neotropical phyl-
males. Awbrey (1978) tested the hypothesis of alterna- lostomatid bat, Trachops cirrhosus, not only responds to
tion of cali rates by analyzing the responses of male Hy/a anuran vocalizations but distinguishes specific calis and
regula to playbacks of recorded calis, and found that the avoids the distasteful Bu/o fyphonius (M. Ryan and Tut-
observed patterns of phase shifting, inhibitíon of simul- tle, 1983). The same species of bat shows greater attrac-
taneous calling, and spatial distributíon of individuáis within tion to complex than to simple advertisement calis of
a chorus supported the hypothesis that social interrac- Physa/aemus pustulosos (M. Ryan et al., 1982); this led
tions minimize cali interference among neighboring males. Rand and M. Ryan (1981) to postúlate that the com-
On the other hand, synchronous calling by numerous plexity of advertisement calis in P. pustulosus evolved to
individuáis occurs in some explosive breeders, such as allow males to effect a compromise between maximizing
Bu/o americanas (Wells, 1977a), Bombina bombina and the ability to attract mates and minimizing the risk of
B. variegata (Lórcher, 1969), and Rana escu/enta (Wahl, predation. A similar response occurs in the hylid Smilisca
1969). Rhythmic bursts of vocal activity are effective in si/a to the same species of bat, but this species of frog
attracting females to a breeding site where males obtain seems to maximize its calling effectiveness by synchro-
mates by active searching rathcr than by individual at- nized calling in the vicinity of waterfalls (Tuttle and M.
traction by vocalization. Ryan, 1982). Snakes are common predators on frogs,
In choruses of some species, certain individuáis may but their most sensitive auditory reception range of
initiate choruses more frequently than do others (Fig. 4- 100-200 Hz (Wever and Vernon, 1960) is below the
16). Experiments with Hy/a regula showed that females dominant frequencies emitted by most frogs; therefore
consistently approached the loudspeaker that was used snakes may not be attracted by long-distance airborne
to initiate each trial of conspecific playbacks, even though acoustic signáis produced by calling frogs. However,
the initiation of calling was varied among four speakers aquatic snakes may respond to underwater vibrations
(Whitney and Krebs, 1975). Wells (1977a:675) cau- caused by calling frogs, such as many species of Rana.
üoned against the inference of dominance in these situ- Gorzula (1978) reported that Caimán crocodi/us feeds
ation: "If 'chorus leaders' do enjoy greater mating suc- on three species of frogs that cali from the water in the
cess than other frogs, this does not necessarily imply that Venezuelan llanos; the caimans move from large bodies
females 'prefer' these males because they make 'better' of water to the temporary pools where the frogs are call-
mates. The most successful males may be those that out- ing, presumably in response to their vocalization. Many
signal their competitors and are. therefore easiest to lócate large species of anurans feed on other frogs, but it is
in a large chorus. . . . Chorus leaders are sometimes re- unknown if these rather sedentary species (e.g., Cera-
ferred to as 'dominant' individuáis, and ordered se- tophrys and Pyxicephalus) respond to vocalizations by
quences of calis have been termed 'hierarchies'. . . . potential prey. Notable exceptions are the observations
However, there is no evidence that call-order is deter- of a Bu/o marinus moving to calling Physa/aemus pus-
mined by agonistíc encounters among males, so there is tulosus and eating them (R. Jaeger, 1976), and of a Rana
no reason to suppose that organized choruses are anal- catesbeiana being attracted to the distress calis of young
ogous to dominance hierarchies of other animáis." individuáis of R. b/airi andR. catesbeiana (A. Smith, 1977).
Nonetheless, the factors that influence certain individuáis
to initiate choruses remain unknown. Reciprocation Calis
Little is known about the energeüc costs of vocaliza- These calis emitted by females are known to occur only
tion. Experiments on the leptodactylid Physa/aemus pus- in the European discoglossid A/ytes obsteíricans (Heinz-
tulosas revealed rates of oxygen consumption to be four mann, 1970) and the Mexican leptodactylid Tomodac-
times greater in calling males than in males resting by ty/us angustidigitorum (Dixon, 1957). In both cases males
day (Bucher et al., 1982). respond by changing their advertisement calls-softer notes
Another cost of vocalization is the attraction of poten- in A/ytes and a change from peeps to a trill in Tomo-
tial predators (M. Ryan et al., 1981). Certainly some dacty/us.
mammals, such as raccoons (Procyon lotor), must be
attracted to calling sites by vocalization; opossums (Phi- Reléase Calis
lander opossum) are known to lócate frogs acoustically These are agonistic signáis emitted by a frog when am-
(Tuttle et al., 1981). Various tropical bats are known to plexed by another; they are accompanied by distinct vi-
 Vocalization
tations of the body wall. These accentuated respiratory 103
wbtations, which are produced by both males and fe-
Males, expel air in short bursts; thus, the reléase calis
asually are a series of short chirps and nave notably dif-
ierent acousüc properties than the advertisement calis 6-
(fig. 4-17). As noted by Aronson (1944), the reléase calis
and warning vibrations most commonly are produced by
males when amplexed by an indiscriminate male, but 4-
fcese reléase signáis also are produced by spent females.
Therefore, these signáis may inform the amplexing male
fíat the partner is incapable of reproducing. Rapid re- 2-
léase presumably is advantageous, for energy is con-
served and gametic wastage is prevented.
Reléase calis have been reported for most groups of
fcogs. but they are unknown in microhylids (Bogert, 1960). 0.2 0.4
Reléase calis and vibrations are produced by many frogs Time in Seconds
fíat lack advertisement calis: Pleurodema bufonina Figure 4-17. Reléase cali of Bufo valliceps. Narrow-band (45-Hz)
(Duellman and Veloso, 1977), Hemiphractus fasciatus display. Compare with advertisement cali in Figure 4-13E.
ÍMyers, 1966), and toads of the Bu/o bóreas and B.
spmu/osus groups (L. Brown and Littlejohn, 1972; Penna
»d Veloso, 1981).
Genetic control of the reléase calis is implicated by
evidence that the pulse rates of the reléase vibration in
natural hybrids berween Bu/o houstonensis and B.
6-
woodhousii are intermedíate between those of the pa-
rental species (L. Brown and Littlejohn, 1972).

Distress Calis
The loud, explosive distress calis given in response to
acute disturbance or grasping by a potential predator are
produced by either sex and someümes even newly me-
tamorphosed young (Sazima, 1975), and are acoustically
dissimilar to the advertisement calis (Fig. 4-18). Distress
calis resultíng from disturbance possibly provide a warn- 0.2 0.4
ing of potential danger to other individuáis. A person Time in Seconds
walking along the margin of a pond in the northeastern
United States might disturb a green frog, Rana clamitans, Figure 4-18. Distress cali of Leptodactylus pentadactylus.
which emits a loud cry as it leaps into the water; usually Narrow-band (45-Hz) display. Compare wíth advertisement cali ¡n
Figure 4-14A.
several frogs nearby also will take refuge.
Screams are emitted by some frogs when they are
grasped by predators. It is unknown if these calis convey and Bu/o calamita (E. Weber, 1978). The distress cali
any information to other frogs, and it is doubtful if these also may be accompanied by a warning display, as noted
screams have any effect on an ophidian predator. How- in the Andean marsupial frog, Gostrotheca hetenae; a
ever, loud vocalizaüons may sufficiently surprise a mam- disturbed female emitted a long series of loud buzzes and
malian or avian predator so that the prey may be released displayed the bright bluish-green tongue and buccal lin-
momentarily, thereby allowing the frog to escape. This ing. When disturbed, the large Chilean frog, Caudiver-
certainly is the case with uninitiated frog collectors cap- bera caudiverbera, emits a loud cali and lunges forward
turing their first South American jungle frogs, Leptodac- with its mouth open (Veloso, 1977). The distress cali of
ty/us pentadactylus. Upon being seized, these large frogs Bufo calamita is followed immediately by the appearance
sometimes emit a loud scream reminiscent of that given of a white muCous secretíon over the enüre dorsal surface
by a cat in distress. Australian tree frogs, Litaría caerulea, of the body (E. Weber, 1978). Tyler (1976:143) reported
sleep in hollow branches by day; monitor lizards (Var- that the Australian Cyc/orana cu/tripes "seems to exhibit
anusj enter the hollows and disturb the frogs, which emit a rather nervous disposition for it screams in anticipation.
piercing screams (Tyler, 1976). When you reach to pick one up it commonly opens its
Distress calis usually are emitted with the mouth open, mouth wide, screams piercingly and simultaneously jumps
but their production with the mouth closed has been absolutely vertically high into the air to fall in a heap on
reported in Rana catesbeiana (J. Hoff and Moss, 1974) the ground where it had been sitting."

f
LIFE HISTORY
ABIOTIC FACTORS by about one-third of its duration and the interval be-
AFFECTING VOCALIZATION tween calis being reduced by about one-half (H. Schnei-
der, 1977). Zweifel (1959) analyzed 22 recordings of one
Temperatura individual of Bombina variegata at temperatures from
Many frogs in températe regions breed in the early spring 16.8°C to 25.6°C, and found that repetition rate and
when temperatures are highly variable; because frogs are pitch (frequency) have a significant positive correlation
ectotherms, it is expected that the acousüc properües of with temperature, but that the duration of the cali is nega-
their calis will vary wíth temperature. In the cricket frogs, tively correlated with temperature. These results are alike
Acris crepitans, cali rate increases significantly at higher in that spectral frequencies, pulse repetition rates, and
temperatures (A. Jackson, 1952). A statistically significant note repetition rates are directly related to temperatures,
positíve correlation between temperature and cali rate whereas durations of calis are inversely related. Thus, if
and a negativo correlation between temperature and a frog normally produces 10 notes in a cali and those
duration of cali exist in two species of chorus frogs, Pseu- notes are produced more rapidly at higher temperatures,
dacris (Bellis, 1967). Temperature-dependent changes in the duration of the cali will be shorter (Fig. 4-19).
pulse rate, dominan! frequency, and cali duration of the There is a positive correlation between temperature
advertisement cali of Hyla versicolor were demonstrated and frequency of contraction of larygeal muscles in Hyla
by W. Blair (1958). Similar results were obtained in anal- arbórea (Manz, 1975); thus, it seems as though temper-
yses of reléase calis of several species of Bu/o (L. Brown ature is affecting the basic sound-producing mechanisms
and Littlejohn, 1972). A high positive correlation exists of the frogs. H. Gerhardt (1978) experimented with re-
between pulse rate and temperature in two species of sponses by gravid females of the tree frog, Hyla versicolor
Bufo and in their natural hybrids (Zweifel, 1968). to advertisement calis produced at different tempera-
In the European tree frog, Hyla arbórea, an increase tures. He found that females responded to calis with tem-
of 10°C results in the advertisement cali being shortened perature-dependent properties produced at temperatures
similar to their own, and concluded that vocalization and
recognition systems are affected by temperature in a
qualitatively similar way, a phenomenon termed tem-
8- perature-coupling. This conclusión is supported by Moh-
neke and H. Schneider (1979) and Hudl and H. Schnei-
der (1979), who found that temperature affected auditory
thresholds in four European species of frogs.

Habitat Interference
Other environmental factors also influence sound pro-
duction in anurans or have an effect on the efficiency of
communication. The humidity of the air and density of
vegetation are importan! in the transmission of sound.
Schiótz (1967) documented qualitative differences in the
acoustic properties of anuran vocalizations in savanna
and rainforest habitáis in westem África. Frogs in open
8- habitáis (e.g., deserte and grasslands) tend to have longer,
more continuous, and lower-pitched advertisement calis
than do those in forests. Low frequencies carry a greater
distance than high frequencies, but high frequencies are
easier to lócate than low frequencies (Konishi, 1970).
One Asiatic and three South American genera of micro-
hylids that cali from the forest floor have high-pitched
calis (C. Nelson, 1973). A compromise between distance
transmission and directional detectability is exhibited by
2- several species of Leptodactyius that modulate frequen-
cies over a short time span (Straughan and Heyer, 1976).
Frogs in open habitats usually have short, intense pe-
riods of breeding at the onset of the rainy season. Indi-
0.2 0.4 vidual frogs may be scattered over wide áreas, but suit-
Time in Seconds able breeding sites may be highly localized. Vocalizations
having acoustic properties enabling the sound to carry
Figure 4-19. Advertisement calis of the chorus frog, Pscudacris
insertara, recorded at Lawrence, Kansas, at different temperatures. long distances are advantageous in attracting mates to
A. 3.9°C. B. 16.7°C. Narrow-band (45-Hz) displays. these breeding sites. Bogert (1960) showed that both
 Vocalization
males and females of Bufo terrestris oriented to record- man and Veloso, 1977), and African Bufo, Acanthixalus,
ings of choruses, and concluded that advertísement calis and Conraua (Tandy and Keith, 1972; Schtótz, 1973)
are significan! in distance orientation and attraction of breed in stíll water but lack advertísement calis. Also,
toads to breeding assemblages. Frogs in closed forest some Rana and Bufo have weak advertísement calis (W.
habitáis tend to have softer, higher-pitched, and discon- Blair and Petrus, 1954; R. Savage, 1961; Altíg and Du-
finuous advertísement calis; this was documented in Asiatic mas, 1971; Geisselman et al., 1971). The absence of
microhylids by Heyer (1971). In a tropical rainforest, it advertísement calis in such anurans possibly is related to
is not uncommon to be within 100 m of a breeding con- the spatíal and temporal pattems of their reproductíve
gregaüon of several species of calling frogs before the behavior, which includes active visual searching for mates
chorus can be heard. For example, the rate of attenuatíon (Wells, 1977a).
of the calis of Centrolenella fleischmanni was doubled in These inferences about the effectíveness and distances
vegetation as compared with open situatíons (Wells and of sound transmission are dependent not only on the
J. Schwartz, 1982). This is in striking contrast to a chorus properties of the acoustic signáis but also on the intensity
made up of Rhinophrynus, Smilisca, and Phrynohyas in and beaming of the calis. Little information is available
open scrub forest in southwestern México; what sounds on these aspects of anuran calis. Lofrus-Hills and Little-
Bke a nearby congregation may be nearly a kilometer john (1971a) found that among seven species of Austra-
away. lian frogs, smaller species have less intense signáis than
Subterranean vocalization presents some problems. do larger species, presumably because of smaller vocal
Acoustíc signáis of high frequency are absorbed readily sacs and body-wall musculature. H. Gerhardt (1975)
by soil parücles, and calis are audible for only a short analyzed intensities of calis of 21 North American anu-
distance. In eight species of fossorial Papuan microhylids, rans and concluded that interspecific differences in inten-
the advertísement calis are characterized by a narrow sity were not clearly related to interspecific differences in
band of dominant frequency at less than 1000 Hz and body size. Similarly, no clear relatíonship between body
one or more short notes with constant amplitude. Men- size and intensities of calis was found among calis of 17
zies and Tyler (1977) suggested that the low frequencies species of African frogs (Passmore, 1981). However, body
are the best transmission bands through the soil and that size, per se, may not be nearly so important as size of
the narrow bandwidths result in greater amplitudes by vocal sac. For example, sound intensities are about equal
the concentratíon of spectral energy to counteract rapid in Bufo amerícanus and B. quercicus; the former is about
attenuation in the soil. four tímes the size of the latter, but the vocal sac is pro-
Frogs that breed in, or along, torrential streams must portíonately much larger in B. quercicus.
compete acoustically with the noise generated by the Data on directionality of vocalizations is inconclusive.
rushing water. For example, short, impulsive, high-pitched Slight reductions in sound intensities from in front of to
calis are characteristic of centrolenids and some dendro- in back of calling males of several species of North Amer-
barJds (Colostethus); members of both groups cali from ican and South African frogs were reported by H. Ger-
the immediate vicinity of rushing streams. Among hylid hardt (1975) and Passmore (1981). However, direction-
frogs in México and Central America, the dominant fre- ality of calis resulted from sound reflection by certain
quencies of the advertísement calis of 19 species that cali calling sites in Eleutherodactylus coqui (Narins and Hur-
from forest ponds are 272-3578 (mean = 1726) Hz, ley, 1982) and Centrolenella fleischmanni (Wells and J.
whereas calis of 25 species that cali from mountain streams Schwartz, 1982). These factors must be taken into con-
are 1275-4300 (mean = 2530) Hz (data from Duellman, sideration in studies of mate attraction.
1970). Some frogs that live along mountain streams have Likewise, there is little information on the distances at
weak voices (e.g., Atelopus, Taudactylus, some species which individuáis can detect conspecific calis. According
of Telmatobius, some hylids) or no voice (e.g., Ascaphus, to Loftus-Hills and Littlejohn (1971a), the small Austra-
some species of Telmatobius, some species of Bufo, some lian myobatrachid Crinia parinsignifera probably cannot
hylids); this may be an altematíve response to the noise detect conspecific advertísement calis at distances of more
level of the streams. than 4 m, but the cali of the larger hylid Litoria ewingii
Stream-dwelling frogs that lack voices usually remain probably is detectable by conspecific individuáis to dis-
at the edges of the streams; they do not need to vocalize tances of 100 m; the same distance of 100 m was de-
in order to attract mates to the breeding sites. In multis- termined for Hyla cinérea by H. Gerhardt (1975).
pecies associations, specific recognitíon may be visual,
tactile, or chemosensory, whereas in monospecific situ-
ations—for example, some high montane regions inhab- INTERSPECIFIC SIGNIFICANCE
ited by Ascaphus, by some Telmatobius, or by some OF VOCALIZATION
Atelopus— critícal specific recognitíon is not necessary.
Some températe and montane species of Bufo (Heusser, Acoustic Interference
1961; Schuierer, 1962; Black and Brunson, 1971; Novak In a multispecies community, males of several species
and D. Robinson, 1975), Pleurodema bufonina (Duell- usually utilize a common site (e.g., pond) for advertise-
LIFE HISTORY
ment calling. Consequently, there is the potential for ample, field experiments by J. Schwartz and Wells (1983)
acousüc interference among calling males of different showed that background noise generated by Hyla micro-
species. Littlejohn (1977:279) emphasized: "Interspecific cephala caused a shift in tíming and kinds of calis given
interactions will involve only the resources of communi- by nearby H. ebraccata; males of H. ebraccata reduced
cation, i.e., competitíon for bandwidth, temporal codes, the cali rate and the proportion of multinote and aggres-
transmission time, and calling sites. In this context, the sive calis at high levéis of calling by H. microcephala.
signáis of non-specifics constitute noise.... Interspecific in-
teractions should thus lead to divergence in acoustic be- Acoustic Niches
havior and signal structure because of presence of these Within large, multispecies communities, synchronously
acoustic, but not reproductive, competitors." calling species usually have distinctive acoustic signáis
Selection for communicative efficiency by reduction of differing from other species in the community by fre-
acoustic interference might be accomplished in the fol- quency and/or pulse rate. Studies of such communities
lowing ways (Littlejohn and A. Martin, 1969): comprising 9 species in Florida (Bogert, 1960), 10 spe-
cies (only hylids) in Costa Rica (Duellman, 1967b),
1. Spectral stratíf¡catión through the partitioning 7 species in Victoria, Australia (Littlejohn, 1977), 15 spe-
of bandwidth into numerous discrete fre- cies atManáus, Brazil (Hódl, 1977), 20 species (all hylids)
quencies. in Amazonian Ecuador (Duellman, 1978), and 13 species
2. Spatial separation through aggregation of in- (all hylids) in Perú (Schluter, 1979) have revealed that
dividuáis into monospecific assemblages or spatial and acoustic partitioning exists in any given com-
uülization of discrete species-specific calling munity at a particular time. Among 15 species in floating
sites. meadows at Manáus, overlap in dominant frequencies
3. Temporal partitioning of calling into species- existed in only 4 species, but these had notably different
specific breeding seasons, definitive discrete temporal properties of the calis (Hódl, 1977). In 7 species
diel periods, or through alternation or anti- calling at a pond in southeastern Australia, phasing of
phony within the same diel period. calis occurred in situations where calling sites and cali
4. Differentiation of species-specific coding pat- frequencies were similar (Littlejohn, 1977). A stepwise
terns of advertisement calis when frequency discriminant functions analysis of cali data from 20 sym-
bands and calling times broadly overlap. patric hylids revealed that fundamental frequency was
the best discriminator, followed by dominant frequency
Differences in acoustic propertíes of advertisement calis (highly correlated with fundamental frequency), pulse rate,
may have evolved in response to selection for minimizing and number of notes; these four properties discriminated
acoustic interference among sympatric and synchronous 96% of the individuáis (Duellman, 1978). In all cases,
breeders, thereby enhancing specific idenüfication. How- species that have the most similar calis exhibited spatial
ever, acoustic differences may have come about inciden- differences.
tally or indirectly through selection for other factors, such Within the limited vocal repertoire of anurans, it is ex-
as body size, which may affect acoustic properties of calis, pected that convergence in advertisement calis would be
such as dominant frequency. a common phenomenon. Striking similarities occur in
Acoustic differences are especially important in main- geographically distant and unrelated species of frogs, such
taining species identities among closely related sympatric as in the North American pelobatids (Scaphiopus), South
congeners. In a review of the advertisement calis of such American leptodactylids (Odontophrynus), and Austra-
species pairs, Littlejohn (1969) found pulse rates usually lian myobatrachids (Notaden), all of which produce
to be distinctive between pairs of species. Cali differen- structurally similar calis while floating on surfaces of tem-
tiation in allopatric and sympatric populations of pairs of porary ponds after torrential rains. Excellent examples of
species has been documented in few cases. In the North convergence in advertisement calis include the African
American microhylids Gastrophryne carolinensis and G. hyperoliids, Afrixalus and Kassina, with many neotropical
olivácea, cali durations, dominant frequencies, and pulse hylids, especially members of the Hyla microcephala,
rates are more distinctive in sympatric than in allopatric leucophyllata, and parviceps groups. Also, calis of Aus-
populations (W. Blair, 1955). In the Australian hylids Li- tralian species of Limnodynosíes and of the Litaría nasuta
toría ewingii and L. verreauxii (Loftus-Hills and Little- group bear strong resemblances to calis of various species
john, 1971b) and in the North American hylids Pseu- of Leptodacty/us and Ololygon, respectively, in South
dacrís nigrita and P. tríseñata (Fouquette, 1975) and Hyla America.
chrysoscelis and H. versicolor (Ralin, 1968), the ranges Moreover, at geographically sepárate sites in the same
in pulse rates do not overlap in sympatric populations, biogeographic realm acoustically similar calis can be heard,
but do overlap in allopatric populations. although the species composition of the communities is
However, in cases of similar calis among species in a partially or completely different. Analyses of acoustic
mixed chorus, vocal interactions may have important ef- properties of 39 species of hylid frogs constituting breed-
fects on the calling behavior of individual males. For ex- ing communities in Brazil, Costa Rica, and Ecuador showed
 Vocalization
that there were four groups of cali types and that species that species sharing morphological and/or biochemical
from each community were included in each group attributes also have structurally similar advertisement calis.
(Duellman and Pyles, 1983). Acoustic properties of anu- In some cases, limitations are imposed on the vocaliza-
ran breeding congregations are analogous to ecological tions by the morphology of the frogs. For example, the
resources; distinct acoustic niches are evident within anu- laryngeal apparatus of pipids is unique, and their vocal-
ran communities, and allopatric species tend to fill equiv- izations are unlike those of any other frogs (G. Rabb and
alen! niches in difieren! communities. M. Rabb, 1963). Atrophy of the middle ear structures is
associated with reduced vocalization in some lineages,
Inhibition such as in some species of the bufonid genus Atelopus
Inhibitory effects of the advertisement cali of one species (McDiarmid, 1971).
on the calling behavior of another sympatric species have With some genera that have been studied acoustically
been documented only in the Australian myobatrachids as well as morphologically, cali structure parallels the
Geocrinia uictoriana and Pseudophryne semimarmorata, morphological groups. Among Mexican and Central
which are broadly sympatric and synchronous breeders. American hylids, some genera and species groups have
Through playback field experiments, Littlejohn and Mar- characteristic advertisement calis, but intergroup relation-
tin (1969) demonstrated that calling activity of males of ships, as defined on morphological characters, are not
Pseudophryne was inhibited upon exposure to calis of always paralleled by the vocalizations (Duellman, 1970).
Geocnnia. Playback of synthetic signáis indicated that Generic and intergeneric groups of neotropical micro-
pulsed notes with frequencies of 1500-2500 Hz had op- hylids are supported by cali structure (C. Nelson, 1973b),
timal inhibitory effects on calling by Pseudophryne. The but the advertisement calis of Asiatic microhylids have
inhibition of calling by Pseudophryne was interpreted as limited usefulness in determining higher phylogenetic re-
a mechanism of reducing acoustic interference and thereby lationships (Heyer, 1971). Morphological groups of South
increasing its efficiency of communication. American Leptodactylus have distinctive advertisement
Similar situations undoubtedly prevail in other com- calis (Straughan and Heyer, 1976). Two groups of spe-
munities. For example, in the upper Amazon Basin Hyla cies of Dendrobates in Central America and northwestern
leucophyllata and H. sarayacuensís are broadly sympatric South America are distinctly different in morphology, skin
and have structurally similar compound advertisement toxins, and cali structure, which also is correlated with
calis; they also utilize similar calling sites and oviposition differences in aggressive behavior in the two groups (Myers
sites. Both are opportunistic breeders after rains, yet cho- and Daly, 1976).
ruses are discrete—not in the same ponds on the same The most exhaustive study of the phylogenetic signif-
nights (Duellman, 1978). However, silent males of one icance of vocalization has been on species of Bufo
species frequently are present in congregations of calling (W. Martin, 1972). Three patterns of amplitude modu-
males of the other species, and a chorus of one species lation are unique to Bufo and to the South American
may be present in a pond where a chorus of the other leptodactylid Odontophrynus. These types of amplitude
species existed a few nights earlier. The presence of tad- modulation are closely correlated with phylogenetic groups
poles of both species in the same pond attests to the based on nonvocal characters. The primitive type of
successful reproduction of both species there. modulation occurs in Odontophrynus and most species
of Bufo in South America, the postulated center of origin
of the genus. Among African Bufo the phylogenetic groups
defined on morphological and biochemical evidence are
PHYLOGENETIC IMPLICATIONS supported by data on cali structure (Tandy and Keith,
OF VOCALIZATION 1972; Tandy and Tandy, 1976).
Presumably, early anuran vocalizations functioned pri- Straughan (1973) argued that certain similarities in vo-
marily for the attraction of mates. As frogs dispersed into cal characteristics could be indicative of relationships at
diverse habitats, environmental factors exerted new kinds the family level. He pointed out that some primitive groups
of selective pressures that influenced acoustic signáis— of frogs (e.g., Cyclorana) have advanced types of calis,
modification of frequency bands, temporal components, in the sense that they have well-developed tuning and
or intensity—for more effective communication. Further- temporal partitioning, whereas North American species
more, frogs in multispecies communities were faced with of ñaña have simple calis. Straughan (1973:326) noted:
the problem of interspecific acoustic interference; thus, "Simplifications of a necessary functional system without
effective communication might have necessitated modi- passing through some peculiar adaptive zone during evo-
fications in the calis. These selective pressures have re- lutionary development...is not very probable." Thus, he
sulted in the diversity of advertisement calis that now exist suggested an early divergence of ranids from primitive
among anurans. Despite this diversity of modifications, it anurans. The complex interactions of acoustic and abiotic
is possible to utilize vocalizations in some limited analyses environments and morphological constraints on the vocal
of phylogenetic relationships. and auditory systems in the evolution of the major groups
Systematic studies of various genera of frogs have shown of frogs render such arguments tenuous at best.
 CHAPTER 5
It is olear that in the Amphibia there epist
patterns of development which transcend
the tajconomic boundaries and appear to
be adaptations in themselves
Stanley N. Salthe and
John S. Mecham (1974)

T he three previous chapters have dealt with the re-

productive biology of amphibians from the internal con-
and a few species of Rana, Bu/o, Triturus, and Ambystoma
(commonly, but erroneously, spelled Amblystoma). The
trol mechanisms of the reproductíve cycles through comparatively small amount of work on amphibians hav-
courtship and egg deposition. This chapter treats the de- ing specialized modes of development has revealed many
velopmental aspects from fertilization through hatching fascinating aspects of development that need to be pur-
or birth. The morphology, ecology, and behavior of lar- sued.
vae are treated in Chapter 6.
Arnphibian development has been investigated exten-
sively by embryologists, who have taken advantage of SPERMATOZOA AND FERTILIZATION
the development of relatively large external eggs for both Productíon and reléase of spermatozoa have been dis-
descriptive and experimental studies. In fact, enüre books cussed in Chapters 2 and 3. Here are treated the struc-
have been devoted to amphibian development (e.g., Rugh, ture of spermatozoa and the actual processes by which
1951, 1962; R. Harrison, 1969). Fox (1984) provided a they penétrate the egg capsules and ova.
thorough account of amphibian morphogenesis. The most
comprehensive treatment of amphibian development Spcrmatozoan Structure
within a broad biológica! context is the work of Salthe The basic morphology of an amphibian spermatozoon
and Mecham (1974). This chapter summarizes amphib- consists of the following structures in a linear, antero-
ian development, including egg and clutch structure, em- posterior sequence (Fig. 5-1).
bryonic metabolism, rates and patterns of embryonic de-
velopment and the process of hatching. Emphasis is placed
on those aspects that have evolutionary and ecological Tai I membrane
Mead Neck Axial rod
significance. Throughout the chapter, reference is made
to developmental stages, which are described in detail in
the section: Normal Stages of Development.
The bulk of the research on embryonic development
has been with species that have aquatic eggs; actually, Acrosomal cap Flagellum
the vast majority of the literature deals with the devel- Figure 5-1. Generalized amphibian spermatozoon showing
opment and experimental manipulations of Xenopus laevis morphological structures.
109
LIFE HISTORY
110

Figure 5-2. Amphibian spermatozoa. A.

Ichthyophis glutinosas. B. Trituras marmoratus.
C. Bufo bufo. D. Ololygon Juscovaria. Not
drawn to scale. A adapted from F. Sarasin and
P. Sarasin (1887-90); B and C from Ángel
(1947); D from Fouquette and Delahoussaye
(1977).

Acrosome. The tip of the head piece is formed by spermatozoa is the presence of a tail membrane in am-
transformation of laminar parte of Golgi bodies during bystomatids that is unknown in other salamanders (Mar-
spermatogenesis. This is properly referred to as an ac- tan and Wortham, 1972). A cytoplasmic droplet contain-
rosomal cap. ing mitochondria migrates from the head to the neck in
plethodontids but remains in the head in other salaman-
Head. The head and acrosome may not be entirely ders. Also, apparently there is a barb on the acrosome
distinct externally in amphibians. The head contains closely in all salamander spermatozoa, but its length and posiüon
packed chromosomes covered by a thin layer of cyto- are variable (Wortham et al., 1982). There are interspe-
plasm. cific differences in lengths of parte of spermatozoa in Am-
bystoma, and spermatozoa of hybrids are intermedíate
Neck or Middle Piece. Formed from cytoplasmic between those of parental species (Brandon et al., 1974);
material, the neck contains one (in salamanders) or two the same is true for species of Hynobius and their hybrids
(in anurans) centrosomes (centrioles) anteriorly next to (Kawamura, 1953). Proportíonal differences in lengths of
the nuclear material of the head and at the proximal end different parís of spermatozoa of plethodontids are con-
of the axial rod or filament. Mitochondria spiral around sisten! with the taxonomy of the group (Wortham et al.,
the axial rod. 1977). The structure of the junction of the head and neck
in spermatozoa is different among genera of salaman-
Tail. The tail is long, usually vibratory, and consiste of drids (Fawcett, 1970; C. Werner, 1970) and among the
an axial rod or filament covered by a very thin layer of species of Ambystoma (Brandon et al., 1974). Similar
cytoplasm, which does not reach to the üp of the tail. differences among plethodontids are consistent with the
The axial rod consiste of several longitudinal fibers with subfamilial groupings, except for Aneides (Wortham et
another fiber spiraled around them and contains the usual al., 1977).
vertébrate microtubule arrangement (nine pairs sur- Striking differences occur in tail structure among anu-
rounding a single median pair). Cytoplasm is expanded rans (Fouquette and Delahoussaye, 1977). Two or more
into a finlike structure, the flagellum, but the distal part tail filamente are present in all primitíve anurans studied
of the axial rod, the end piece, is always naked. The (discoglossoids, pipoids, and pelobatoids). Two tail fila-
cytoplasm may be differentiated into a tail membrane mente occur in some members of the Hylidae and Lep-
posteriorly. The spermatozoa of salamanders and caeci- todactylidae and in nearly all centrolenids and bufonids.
lians have single tails, but in anurans the tail may be Many leptodactylids, most hylids, all pseudids, and nearly
single or double. This normal pattern is modified in Bom- all ranids and microhylids have a single tail. Careful study
bina bombina and B. varíegata, in that the tail is trun- of the structure of the spermatozoa of the species of the
cated and the flagellum is present on the head as well as hylid genus Ololygon revealed interspecific differences in
on the tail (Broman, 1900; Furieri, 1975). the shapes and proportíonal lengths of the head and neck,
The morphology of spermatozoa is highly variable in plus variation in tail structure.
anurans and salamanders (Fig. 5-2); too little is known Resulte of these studies on spermatozoa of relatively
about their morphology in caecilians to make any gen- few taxa suggest that certain morphological characters
eralizatíons. Among the kinds of variation in salamander are consistent with classification and that characters of
 Eggs and Development
úte spermatozoa may contribute to understanding of the its máximum development in about 2 hours after pene- 111
phylogeneüc relationships among groups of amphibians. tration (Elinson and Manes, 1978). In salamanders the
site of spermatozoan entry is marked by a sperm pit
Proteins. The protein structure of amphibian sper- (Fankhauser and C. Moore, 1941).
matozoa is highly variable, like that in fishes and unlike Penetration of the ovum by the spermatozoon serves
that in reptiles, birds, and mammals. Interspecific differ- three functions. First, the egg is activated; second, the
ences in histones were noted for a variety of anurans diploid chromosome complement is formed; and third,
(Kasinsky et al., 1978). Different species of Xenopus and cleavage is initiated. Activation involves elevation of the
their interspecific hybrids can be distinguished by their vitelline membrane, rotaüon of the ovum within the vi-
histones (Kasinsky et al., 1981). Even intraspecific dif- telline membrane, changes in the turgidity of the ovum,
ferences occur in proamines in salamanders (Ando et al., and changes in the surface of the ovum (that is, formaüon
1973). Kasinsky et al. (1978) hypothesized that histone of microvilli or a "pit" where entry was achieved) and
cfiversity in spermatozoa declines in vertébrate evolution elimination of the second polar body. Cortical contraction
as sex determination becomes increasingly chromo- is associated with turgidity and serves to bring the nuclei
somally based. However, this does not explain the di- of the spermatozoon and ovum closer together, thereby
versity of histones in anurans. Histone variation does not bringing about chromosomal association (Elinson, 1975,
seem to be correlated with reproductive modes in anu- 1977). Apparently cleavage is initiated by the presence
rans, for all species studied so far have the generalizad of a centriole from the spermatozoon (Maller et al., 1976);
mode of aquatic eggs and larvae. On the other hand, the acrion of the centriole in organizing a spindle or áster
there may be some phylogenetíc significance, for species is dependen! on activated egg cytoplasm. Also, the sperm
of Rana are grouped together, Scaphiopus is clustered áster is importan! in formation of the gray crescent (Manes
with Bu/o, and Xenopus is closest toNotophthalmus (Ka- and Barbieri, 1976, 1977). The fate of the centrioles pro-
sinsky et al., 1978). duced by the ovum is unknown. Eggs of some species
The biological significance of differences in size and can be sümulated to develop parthenogenetically without
structure of spermatozoa is unknown. Species-specific spermatozoa, and these form normal blastulae.
differences in spermatozoa may be correlated with dif- Amphibian eggs normally are fertilized after reaching
ferences in the structures of egg membranes (Kawamura, Metaphase II. When eggs are inseminated prior to that
1953; C. Nelson and R. Humphrey, 1972). Because there phase, several spermatozoa may enter, but entry does
is a posiüve correlation between spermatozoan head length not actívate the ovum. In anurans the changes in egg
and the amount of nuclear material in plethodontid sal- surface in response to acüvation apparently result in part
amanders (Macgregor and M. Walker, 1973), Wortham from the breakdown of cortical granules; these muco-
et al. (1977) suggested that the long heads (more nuclear polysaccharides are discharged into the perivitelline fluid
material) of plethodontíne spermatozoa may be related and seem to block the entrance of more spermatozoa.
to the evolutionary plasücity of that subfamily. Cortical granules apparently are absent in salamander
eggs, but changes in some of the mucoid capsules upon
Fertilization hydration seem to block the entrance of additíonal sper-
The complex interactions of ova and their mucoid cap- matozoa (McLaughlin and A. Humphries, 1978).
sules with the spermatozoa are both enzymatic and me- As a result of the rapid propagation of the first surface
chanical in the processes of inseminatíon and fertilization. reaction of the egg followed by the second, slower cor-
In amphibians having aquatic eggs, 10 to 15 minutes tical reaction and elevation of the vitelline membrane,
elapse between the first contact of a spermatozoon with only one spermatozoon normally penetrales to the ovum
the egg capsule and fertilization. in those anurans studied. If more than one spermatozoon
Proteolytic enzymes produced by the acrosome of a enters the anuran egg, development inevitable is abnor-
spermatozoon digest the egg capsule and permit me- mal and the embryo is not viable. Several spermatozoa
chanical penetration of the spermatozoon into the ovum may enter the ovum in salamanders, but only one of
(Penn and Glenhill, 1972). Differences in the size of holes these particípales in the development of the zygote; the
digested in egg capsules in various species of Hana and others degenerate. The distinction of monospermy in
Bu/o indícate that enzymatic or substrate traits are spe- anurans and polyspermy in salamanders may be artificial,
cies-specific (Elinson, 1974). for the polyspermic condition is common to large-yolked
The site of entry of the spermatozoon into the ovum eggs, such as those of some mollusks, reptiles, and birds.
determines the future plañe of bilateral symmetry, and The number of spermatozoa entering large-yolked eggs
this site eventually comes to be on the ventral side of the of anurans that have direct development is unknown.
embryo. Penetration is effective only in the animal hemi-
sphere. The gray crescent forms opposite the point of
entry; gastrulaüon is initiated at the gray crescent. In those EGG STRUCTURE
anurans studied, spermatozoa entering the ovum cause Although all amphibian eggs are basically the same in
a localized change in the surface of the ovum, as a clump possessing layers of semipermeable membranes sur-
of microvilli develop; this cytoplasmic differentiaüon reaches rounding the ovum, there is much interspecific variation
LIFE HISTORY
in the disposition of individual eggs within clutches, such baírachus nata/ensis (C. Pope, 1931; A. H. Wright and
as sizes, and number and arrangement of capsules. Fur- A. A. Wright, 1949; Alcalá, 1962; Wager, 1965); and
thermore, various physicochemical propertíes of the eggs some species of the microhylid genus Ka/ou/a (Alcalá,
are importan! to their development under different en- 1962).
vironmental condiüons. Single aquatíc eggs are deposited on the surface of the
water by the pipid Hymenochirus boettgerí (Sughrue,
Clutch Structure 1969) and the bufonid Me/anophrym'scus moreirae
Eggs laid in water may be in the form of large clumps (P. Starrett, 1967); underwater by Bufo punctatus (Liv-
representing the entire ovarían complement (e.g., most ezey and A. H. Wright, 1947) and the ranids Hi/debrand-
Rana and many Ambystoma), or the clumps may rep- tia, Pyxicepha/us, and Tomoptema (Wager, 1965); or are
resent only part of the ovarían complement, in which attached to submerged vegetation by many kinds of newts
case the female deposits small pareéis of eggs at different (Bishop, 1941; Thom, 1968), sirenids (Noble and Mar-
sites (e.g., some Hy/a and some Ambystoma). Com- shall, 1932), and frogs such as Xenopus laevis, Kassina
monly clumps of eggs are attached to sticks or vegetaüon senega/ensis (Wager, 1965), Hy/a crucifer (Gosner and
in the water; this serves to maintain the position of the Rossman, 1960), and H. cadauerina (Gaudin, 1965). The
clutch in the pond or stream. attachment of groups of single eggs or small clumps of
The clutches of hynobiid salamanders are deposited eggs by means of gelatinous stalks to the undersides of
as two sacs, one from each oviduct (Thom, 1968), whereas rocks or logs is common among salamanders inhabiting
the aquatic salamanders Cryptobranchus and Amphiuma streams, including Necturus macu/osus (Bishop, 1941),
deposit paired strings of eggs with a constriction of the Dicamptodon ensatus (Nussbaum, 1969a), and pletho-
jelly between each egg (Bishop, 1941; Cagle, 1948). dontíds such as Eurycea bis/ineata, Gyrinophi/us por-
Similar strings of eggs with constrictions are attached to phyriticus, Pseudotriton ruber (Bishop, 1941), and vari-
undersides of rocks in streams by Ascaphus truei (Noble ous species of Desmognathus (Organ, 1961). Other aquatíc
and P. Putnam, 1931). Toads of the genus Bufo char- or semiaquatíc salamanders, such as Rhyacotriíon o/ym-
acteristically deposit eggs in paired strings, one from each picus (Nussbaum, 1969b) and Eurycea muttiplicata (P.
oviduct, as do the bufonids Ate/opus uarius and Dendro- Ireland, 1976), deposit unstalked single eggs under rocks
phryniscus minutus (P. Starrett, 1967; Duellman and or in crevices.
J. D. Lynch, 1969) and myobatrachids of the genus Neo- The terrestrial eggs of some bolitoglossine plethodon-
batrachus (Watson and A. Martín, 1973). Clutches in the tids are in strands with constricted jelly between each egg
form of a film with all of the eggs at the surface of the (McDiarmid and Worthington, 1970), whereas the ter-
water are characteristic of many kinds of frogs that de- restrial eggs of other bolitoglossines, some plethodon-
posit in still, shallow water. These include hylids of the tínes, and Ambystoma are unstalked and adherent to one
Hy/a a/bomarginaía and H. boans groups and species of another, as are the terrestrial eggs of anurans. Strands of
Litoria, Osteocepha/us, Osteopi/us, Phrynohyas, and terrestrial eggs with constrictions are characteristic of some
Smi/isca (Duellman and A. Schwartz, 1958; Bokermann, caecilians (M. Wake, 1977a) and Alytes obstetricans
1965a; Tyler and M. Davies, 1978a); ranids such as Rana (Boulenger, 1897). Many plethodontine salamanders have
catesbeiana, c/amitans, cancriuora, íimnocharis, Ptychad- stalked eggs attached to the roof or walls of underground
ena oxyrhyncha, Ptychadena porosissima, and Phryno- chambers; stalked terrestrial eggs are unknown in anu-
rans.
Egg clutches of anurans also include foam nests; these
are on land or in water in many genera of myobatrachids
and leptodactylids and in trees among rhacophorids and
Perivitelline Outer
capsule
hyperoliids. Centrolenid and phyllomedusine hylids, plus
chamber
some other frogs, have clutches of eggs adherent to vege-
tation above water (see Chapter 2 for discussion and
references).

Ovum Egg Morphology

The ovum of all amphibians is enclosed in a thin, tough
membrane—the vitelline membrane (fertilization mem-
brane or chorion of many embryologists). The vitelline
Vitelline Inner membrane is proteinaceous and semipermeable and is
membrane capsules produced by the ovary (Townes, 1953; Wartemberg and
W. Schmidt, 1961; Salthe, 1965). It is surrounded by a
series of concentric capsules secreted by the oviducts (Lofts,
Figure 5-3. Diagrammatic generalized amphibian egg showing
membranes and capsules. The mucoid capsules vary in number, 1974) (Fig. 5-3). The egg capsules are composed of acidic
thickness, and viscosity. or neutral mucopolysaccharides and mucoproteins (A.
 Eggs and Development
Humphries, 1966; Freeman, 1968); in some species sul- 113
fated mucopolysaccharides are present in some cap-
sules—only the innermost ones in Notophthalmus viri-
descens and Rana pipiens (A. Humphries, 1970; Steinke
and Benson, 1970). Histochemical tests have revealed
Ihat various regions can be distinguished in the oviducts
of some anurans (Shaver et al., 1970) and some sala-
manders; each of these regions produces a different egg
capsule (see Salthe and Mecham, 1974, for examples
and references). The number of oviducal regions and
resultant number of egg capsules vary interspecifically
(Salthe, 1963).
The innermost capsule of salamander eggs liqúenes
soon after deposition; thus, the ovum, surrounded by the
vitelline membrane, floats freely in a capsular chamber.
In most frogs the ovum is restrained by the viscosity of
the innermost capsule (Salthe, 1963). Rotation of the
ovum occurs almost instantaneously in salamanders,
whereas in anurans without a capsular chamber, rotation
requires several minutes. Eggs of several anurans (A/ytes,
Discog/ossus, Pipa, and Eleutherodactylus) are like those Figure 5-4. Diagrammatic rcpresentation of amphibian eggs.
oí salamanders in that a liquid capsular chamber devel- A. Dicamptodon ensatas (Nussbaum, 1969a). B. Pseudoeutycea
ops soon after deposition (Salthe, 1965); a similar cham- nlgromaculata (McDiarmid and Worthington, 1970). C. Scaphiopus
bombífrons (Hoyt, 1960). D. Alytes obstetricans (Salthe, 1963).
ber is present in the caecilian Ichthyophis glutinosus Redrawn from sources cited. Scale = 5 mm. Small scale refers to
(Breckenridge and Jayasinghe, 1979). In plethodontid A; large scale refers to B, C, and D.
salamanders, Pipa, and Eleutherodactylus the chamber
is small at first and increases in size only late in devel-
opment, but in other salamanders, Discog/ossus, and A/- large eggs have direct development; the largest of these
ytes the chamber is essenüally expended fully shortiy after are the eggs of Aneides lugubrís, in which the ovum may
deposition. be 7.4 mm and the outer capsule 9.5 mm in diameter
Salthe (1963) identified as many as eight capsules in (Stebbins, 1951), and Batrachoseps wríghti in which cap-
salamander eggs and noted that firm capsules existed sules are 9 to 10 mm in diameter in later stages (Stebbins,
between soft ones. Homologous capsules identified among 1949a). Eggs of B. wríghti in early stages of development
salamanders indícate that the eggs of Ambystoma are like have ova 5 to 6 mm and capsules about 8.5 mm in
those of Hynobius, except that the two outermost cap- diameter (Tanner, 1853). Ovarían eggs of Phaeognathus
sules of the latter are absent in Ambystoma. The eggs of hubrichti are 5 to 7 mm in diameter (Branden, 1965).
other salamanders have fewer capsules. With the excep- The smallest eggs among salamanders are those of newts
tion of some primitive frogs, such as A/ytes and Pipa, (Notophthalmus uiridescens and Triturus vulgaris), in which
anurans have fewer capsules than salamanders (Fig. the ova are 1.5 mm in diameter and the ovoid capsules
5-4). The greatest variation is among aquatic anurans, 2.4 by 3.6 mm (Bishop, 1941; G. Bell and Lawton, 1975).
and in some species (e.g., Rana catesbeiana) the egg The largest known anuran ovum is 12 mm in diameter
consists solely of an ovum, vitelline membrane, and one with a capsular diameter of 14 mm in the hylid marsupial
capsule. The eggs of egg-brooding hylids, which hatch frog, Gastrotheca cornuta, which has direct development
into tadpoles or froglets, lack a liquefied inner chamber, (Duellman, 1970). Some frogs having direct develop-
have only two capsules, and retain a vitelline membrane ment have proportionately large capsules; for example,
until hatching. Salthe (1963) was unable to find any ob- Pipa pipa has an ovum diameter of 6 mm and a capsule
vious correlations between detailed strucrure of the eggs of 10 to 12 mm (G. Rabb and Snedigar, 1960). The
and environment, except that nonaquatic eggs tend to largest capsules known among aquatic eggs are 15 mm,
have thinner but fewer capsules. Terrestrial eggs also tend produced by Rana spinosa, in which the ovum is only
to have tougher outer capsules; many of these are stícky. 3.37 mm in diameter (Dubois, 1975). The smallest known
The sizes of ova and the capsules are highly variable. amphibian eggs are produced by the pipid Hymenochi-
The largest amphibian eggs known are those of the cae- rus boettgerí, in which the capsule is 1.5 mm and the
cilian Ichthyophis glutinosus, which attain diameters of ovum 0.75 mm in diameter (G. Rabb and M. Rabb,
35 mm and lengths of 42 mm (Breckenridge and Jay- 1963a) and by the üny hylid Limnaoedus ocularis; the
asinghe, 1979). Among salamanders, the ova of Cryp- aquatic eggs of the latter have ova 0.95 mm and capsules
tobranchus alleganiensis are 6 mm and the capsules 1.57 mm in diameter (Gosner and Rossman, 1960). Other
18 mm (Bishop, 1941). Most other salamanders with frogs, such as some leptodactylids of the genera Physa-
LIFE HISTORY
laemus, Pleurodema, and Pseudopa/udico/a, have equally ish yellow. Some frogs that deposit their eggs on leaves
small ova but capsules that are up to 3 mm in diameter. have palé green yolks; these yolks may be protectively
Hylid frogs producing surface-film clutches also have small colored. This is true for centrolenids, phyllomedusine hy-
eggs—ova of 1.3 and 1.2 mm and capsules of 1.5 and lids, and some hyperoliids.
1.8 mm in Smilisca baudinii and S. cyanosticta, respec-
tívely (Duellman and Trueb, 1966; Pyburn, 1966). Physicochetnical Properties
Amphibian eggs deposited in sites exposed to sunlight The structure of amphibian eggs in combinaüon with their
have melanin deposits over the animal hemisphere, biochemical properües provides a fascinating glimpse at
whereas most eggs deposited in places not exposed to apparently adaptive phenomena. Unfortunately, these
sunlight lack the pigment. Terrestrial eggs that undergo kinds of developmental data are available for few species
direct development and that are deposited in concealed representíng even fewer reproductivo modes, so neither
sites lack pigment, as do the eggs deposited on vegetation generalizations ñor evolutionary trends can be proposed
above water by some species of Hyla, Phyllomedusa, at this time.
Centrolenella, Afríxalus, and Hypero/ius. In each of tríese, The vitelline membrane and perivitelline chamber of
the eggs are adherent to the undersides of leaves or Rana pipiens have been studied in detail by Salthe (1965).
wrapped in leaves, so that the eggs are not exposed to During development there is an increase in the volume
sunlight. Species in the C. fleischmanni group deposit of the perivitelline chamber. This increase is primarily an
unpigmented eggs on the undersides of leaves, whereas osmotic phenomenon with the vitelline membrane acting
other species of Centrolenella have pigmented eggs on as a semipermeable membrane. The rate of increase of
the tips or upper surfaces of leaves. Likewise, all species the volume of the chamber appears to be specific to
of Phyllomedusa that wrap their eggs in leaves have un- developmental stages, but the permeability of the vitelline
pigmented eggs but the species that have exposed clutches membrane to ions does not change during development,
have pigmented eggs. Leptodactylids that construct foam although permeability is modified by changes in the pH.
nests in open water have pigmented eggs but those that The elastic modulus of the vitelline membrane decreases
have nests in concealed sites have unpigmented eggs. at about Stage 15 when the major increase in volume
Not all eggs in concealed sites lack pigment. The eggs of begins. Excess pressure in the perivitelline chamber de-
some salamanders that are deposited in dark places have creases from Stage 15 to hatching. Osmotic pressure in
some pigment in the animal hemisphere, such as Eu- the perivitelline chamber increases owing to excretory
proctus osper (Gasser, 1964), Taricha rivularis (Riemer, producís and secretions by the embryo; primarily these
1958), and Hemidacíy/ium scutatum (Bishop, 1941). The are proteins associated with the hatching enzymes pro-
same is true for some frogs, such as Heleioporus eyrei duced by the frontal glands beginning in Stage 15.
(A. Lee, 1967), Notaden nichollsi (Slater and Main, 1963), The mucoid capsules surrounding the ovum and vi-
Cohstethus subpunctatus (Stebbins and Hendrickson, telline membrane protect the developing embryo from
1959), Rana eueretti (Alcalá, 1962), and R. spinosa (C. injury, fungal infestation, and ingestión; the outermost
Pope, 1931). Intraspecific variatíon in the amount of pig- capsule provides support for the ovum by fastening it to
mentation occurs in eggs of newts wrapped in leaves in some object. It has been suggested that the capsules act
water exposed to sunlight, such as Notophthalmus viri- as lenses, focusing rays of the sun on the ovum, thereby
descens (Bishop, 1941), Triíurus palmatus, and T. vul- increasing the temperature of the eggs (Bragg, 1964).
garis (Hamburger, 1936). However, measurements of the refractive Índices of the
The occurrence of melanin in eggs exposed to sunlight capsules of Ambystoma macu/atum and Rana sylvatica
suggests that the melanin may functíon to protect the revealed no significant refraction at the water-capsule
embryo from ultraviolet radiaüon or to increase the tem- surface or berween capsules (Comman and Grier, 1941).
perature of the egg through greater heat absorbtion. Cer- Immediately after egg deposition, the capsules swell by
tainly, pigmented eggs will absorb more heat when ex- the uptake of water. The ionic concentration of the water
posed to sunlight than will unpigmented eggs but the affects the rate and extent of capsular swelling. In the
latter are never deposited in áreas exposed to sunlight. eggs of Rana temporaria, there is a strong negative cor-
Furthermore, heat retention seems to be correlated with relation between the size of the capsules and ionic con-
the shape of the egg mass (see following sectíon). Ex- centration (Beattie, 1980). Similar results were obtained
perimental exposure of eggs of Ambystoma mexicanum for R. pipiens (T. Lee, 1964) and for Bu/o bu/o (Kobay-
(Sergeev and Smirnov, 1939), Triturus alpestrís (Kraft, ashi, 1954). The optimum pH for swelling of eggs of
1968), Xenopus laevis (Gurdon, 1960), and Rana pi- R. temporaria is 6.5 and for those of B. bu/o, 6.4 to 6.8.
piens (Higgins and Sheard, 1926) to intense ultraviolet The aquatic eggs of Rana sphenocepha/a, sylvatica,
irradiation caused mortality and abnormal development and temporaria retain heat more effectively than the sur-
of the eggs. The darkly pigmented eggs of Rana tem- rounding water (Hassinger, 1970; Beattie, 1980). In
poraria are more resistant to radiaüon than the paler eggs R. temporaria, heat retention is much greater in larger
of R. escu/enta (Beudt, 1930). eggs than in smaller ones. If this correlation prevails in-
Amphibian yolk usually is creamy yellow or palé gray- terspecifically, it may account in part for the variation
 Eggs and Development
observed in the sizes of capsules relaüve to the ova in fel, 1968b). The importance of the development on the
many amphibians. Thus, species that deposit their eggs surface of the eggs of Hy/a rosenbergi was demonstrated
ir cold water tend to have proportíonately much larger by Kluge (1981), who found that survivorship of eggs
capsules than those in warm water. For example, cal- was extremely low when eggs were placed on the mud
ailations of the ratío of total egg diameter to ovum di- at the bottom of nests where the oxygen tensión was
arneter from measurements given in the literature show low.
a range in Hana from 1.60 for R. cancrivora, which de- Despite the relatively tough outer capsule of terrestrial
posits its eggs in a surface film on lowland ponds in the amphibian eggs, the eggs are readily susceptible to de-
PhiHppines (Alcalá, 1962), to 4.06 in R. japónica, an hydration. Eggs take up moisture from the damp sub-
eariy breeder in cold ponds in Japan (Okada, 1966), and strate and lose moisture to the drier air. Moisture con-
475 in R. spinosa, which places its eggs in cold Hima- tained within the egg capsules provides a reservoir for
fayan streams (Dubois, 1975). Similarly, within hylids the the developing embryos. Terrestrial egg masses of Pleth-
latios are comparable—1.5 for Smilisca cyanosticta and odon cinéreas and Eleutherodactylus portoricensis can
L6 for Hy/a rosenbergi, which deposit eggs as surface lose up to 12% of their hydrated weight without affecüng
flms on warm water in the American tropics (Pyburn, viability (Heatwole, 1961; Heatwole et al., 1969). The
1966; Kluge, 1981) to 4.4 for Pseudacris brachyphona, size of the capsules relaüve to the ovum and therefore
which deposits clumps of eggs in cold ponds (N. Green, the amount of water contained in the egg seem to be
1938). important factors in the ability of terrestrial eggs to with-
Distinctly different thermal propertíes exist between stand dehydratíon. Larvae of the myobatrachid frog
giobular and surface-film egg clutches. The globular egg Geocrinia u/cíoriana can survive up to 4 months within
masses deposited in still, cold water by some Rana retain the capsules of the terrestrial eggs before the nests are
heat and consequently are warmer than the surrounding flooded (A. Martin and A. Cooper, 1972). These eggs
water. Temperatures of egg masses of R. temporaria and can lose up to 90% of their hydrated weight without
R. sphenocephala were 0.63°C warmer than the water affecting larval viability. In egg masses that are not flooded
(R Savage, 1961; Hassinger, 1970); masses of R. syl- for several weeks after Stage 26 is reached, the individual
vatica in Alaska were 1.0°C, and in New Jersey, 1.6°C, capsules break down and fuse into one homogeneous
warmer than the water (Herreid and Kinney, 1967; Has- jelly mass. This large mass presents less surface área pro-
singer, 1970). However, in the absence of insolatíon, portional to entire volume than do individual eggs, and
temperatura differences become much less (Zweifel, this reduces dehydratíon. Presumably the breakdown of
1968b). If heat retention is dependent on the size of the the capsules is caused by accumulatíons of hatching en-
mass, communal egg deposition, as reported for R. tem- zymes produced by the frontal glands of the embryo.
poraria and R. sylvatica by R. Savage (1961) and R. D. The arboreal egg masses of some tree frogs of the
Howard (1980), respecüvely, would result in higher tem- genus Phyllomedusa are encased in leaves, and each
peratures for the developing eggs. Actually, egg masses group of embryonated eggs is supplemented by many
in the center of communal masses deposited by R. syl- eggless capsules containing metabolic water (Agar, 1910;
vatica are warmer than peripheral masses and have greater Pyburn, 1980a). Experiments with eggs of P. hypocon-
survivorship to hatching (Waldman, 1982a). Conversely, drialis by Pyburn revealed that the leaves protect the eggs
the surface film clutches of R. catesbeiana and Hy/a ro- from desiccation and that the eggless capsules provide
senbergi dissipate heat, and their temperatures are 0.84°C water for the embryonated eggs.
and 0.40°C lower than the surrounding water (M. Ryan, In the aquatíc foam nests of some leptodactylid and
1978; Kluge, 1981). myobatrachid frogs, the outer capsules of the eggs are
Oxygenation of eggs is critícal to their development, shared in common with water, air, and seminal fluid. In
and there is a continua! increase in oxygen consumption some cases the outer surface of the foam nest exposed
during development (Salthe and Mecham, 1974). How- to air becomes dry and crustlike. Terrestrial and arboreal
ever, in ñaña temporaria at least, there is no correlaüon foam nests commonly have dry outer surfaces that pro-
between the rate and extent of swelling of the egg cap- vide an effectJve protectíon against dehydratíon of eggs
sules and the amount of dissolved oxygen in the water in the moist interior of the nest (Coe, 1974). The foam
(Beattíe, 1980). Eggs deposited as a surface film are nest also may be effective in maintaining lower devel-
adaptive with respect to meeüng the oxygen needs of the opmental temperatures in otherwise warm water, as noted
embryos (Moore, 1940). Cool water contains more dis- for Physalaemus enesefae by Gorzula (1977).
solved oxygen, and the eggs in the middle of a globular The mucoid capsules seem to provide some protectíon
but porous mass obtain sufficient oxygen, but in warm against ingestión by predators. Larger, firmer capsules
water with a low oxygen tensión, surface films provide seem to be a deterrent to predatíon by small fish (Grubb,
máximum exposure for each egg. The small egg masses 1972). Experiments on predatíon of eggs of Ambystoma
of Scaphiopus and strings of eggs produced by Bu/o also maculatum by D. Ward and Sexton (1981) showed a
are adapted to warm water because they allow more significant increase in predation associated with the re-
exposure of individual eggs to surrounding water (Zwei- moval of the capsules. Some amphibian eggs have toxic
LIFE HISTORY
and noxious properties. Eggs of Taricha and Ate/opus foothold enabling sperm to penétrate to the ova (Kam-
contain an effective neurotoxin, tarichatoxin (tetrodo- bara, 1953), substantive evidence points to antigen-an-
toxin) (Mosher et al., 1964; Pavelka et al., 1977), and tibody-like reactions between jelly and sperrn. Regional
those of some species of Bu/o are highly toxic to reptiles differences in antigens in anuran oviducts are correlated
and mammals (L. Licht, 1968), as well as to fishes and with the effective fertilization of the eggs (Barch and Shaver,
other anurans. Fishes tend to avoid most toad eggs in 1963). The jelly also may affect the maturatíon of the
nature; thus, some noxious quality seems to be associ- eggs and may have mechanical and possibly even nutri-
ated with the toxicity. tive significance during cleavage (A. Humphries, 1966).
Egg capsules must be present for fertilization and The progressive increase in fertilization and ability to hatch
hatching to occur. Eggs taken from the coelom or prox- as eggs descend the reproductive tract seems to be at-
imal part of the female reproductive tract are not capable tributable to the increase in the amount and composition
of being fertílized in Bu/o bu/o (Kambara, 1953), B. me- of jelly on the eggs. The limited information on the his-
/anogaster (K. Low et al., 1976), and Cynops pyrrho- tochemical complexity of oviducal secretions and the an-
goster (Nadamitsu, 1957). The rate of ferülization in- tigenic materials in the jelly layers suggests that: (1) some
creases as the number of jelly layers accumulates on the components in the jelly layers are essential for fertiliza-
ova as they pass down the oviduct in Notophtha/mus tion; (2) these include both species-specific attributes and
uiridescens (McLaughlin and A. Humphries, 1978) and components shared with congeners; and (3) there is a
B. me/anogoster (K. Low et al., 1976). Furthermore, ex- regional distribution of these components in the oviduct
perimental envelopment of ova (removed from the upper (Shaver et al., 1970).
part of the tracts) with jelly resulted in eggs capable of
being fertílized in Taricha torosa (Good and J. Daniel, EGG DEVELOPMENT
1943) and Rana pipiens (Subtely and Bradt, 1961). The The development of amphibian eggs has been the sub-
innermost capsules are necessary for fertilization in Hyla ject of study and experimentation by embryologists for
japónica (Katagiri, 1963) and various North American more than a century. The massive amount of literature
Bu/o, Hyla, and Rana (Aplington, 1957). In B. arenarum is summarized adequately in texts, such as B. Balinsky
at least, substances diffused from the egg capsules into (1960). Anuran development is described thoroughly by
the surrounding water result in a positíve reaction by Rugh (1951), who also treated experimental embryo-
conspecific sperm (Barbieri, 1976). logical work on amphibians in detail (Rugh, 1962). This
Egg capsules also are importan! to the ability of eggs section is concerned with those comparative aspects of
to hatch. This ability depends on the number of jelly amphibian development that have evolutionary and eco-
coats. Although the jelly might provide a mechanical logical significance.

Figure 5-5. Fetal teeth of a

caecilian, Gymnopis multiplícate,
that function as scraping organs in
the oviduct. Photo by M. H. Wake.
 Eggs and Development
Table 5-1. Comparison of Caloñe Utilization Between Fertilization and Hatching ¡n Four Species of Amphibians* 117
Total length of Honra of Percent of lipids
Species Calories hatchlings (mm) development inyolk
Bu/o bu/o 0.528 4 82 20
Rana pipiens 0.560 6 10
Ambystoma mexicanum 1.710 11 204 29
Andrias japonicus 136.450 14 650 35
«Data from Salthe and Mechara (1974).

Embryonic Metabolism maintain an embryo having a longer duratíon of devel-

Amphibian embryonic metabolism was summarized by opment. Lipids are a major source of energy during de-
Salthe and Mecham (1974). The emphasis here is on velopment; the longer duration of development and larger
nutrition, respiraüon, and elimination of nitrogenous hatchlings in salamanders, as compared with anurans,
wastes. are the result of not only larger yolks but proporüonately
more lipids in the yolk. However, caloñe contents of eggs
Nutrition. With the exception of most viviparous taxa, of three species of Ambystoma vary intrapopulaüonally;
amphibian embryos obtain all nutrients for their devel- the range is 16.5 to 29.0 calories per egg in A. tigrinum
opment, at least to hatching, from the egg yolk. Although (Kaplan, 1980b). Embryos of all three species require
Eleutherodactylus jasperí gives birth to live young, which 1.45 calories to hatch, regardless of ovum size, hatchling
develop entirely within the oviducts, the nutrients for the size, or temperature.
entire embryonic development are provided by the yolk During the development of Ambystoma mexicanum,
and not maternal tissues (M. Wake, 1978). Likewise, pipid fats appear to be utilized early in development, with car-
and hylid frogs that carry developing eggs on their backs bohydrates becoming increasingly importan! through
or in pouches provide no nutrients to the embryos; main- gastrulation stages, after which fats are utilized again; only
tenance of the same dry weights of eggs throughout de- during the later stages are proteins the primary energy
velopment indicates that there is no addiüon of nutrients source (Ltóvtrup and Werdinius, 1957). However, tem-
(del Pino et al., 1975; Weygoldt, 1976b). perature influences differential utílization of energy sources;
The majority of viviparous amphibians are caecilians; at lower temperatures, embryos of A. mexicanum tend
three of the five families contain species known to bear to uülize proteins, whereas at higher temperatures fats
hving young (M. Wake, 1977b). Fetuses of caecilians are the primary energy source. There is virtually no uti-
quickly exhaust their yolk supply, hatch from the egg lization of glycogen in Bu/o arenarum (Barbieri and Sal-
membranes, and obtain nourishment from the female by omón, 1963) or Rana temporaria (Brachet and Need-
ingesting secretions and epithelial tissue from the lining ham, 1935) until gastrulation, at which time glycogen is
of the oviduct. Fetal caecilians have deciduous teeth that used at an ever-increasing rate.
are specialized for scraping the lining of the oviduct (M.
Wake, 1976) (Fig. 5-5). Respiration. The presence of external gills in some
Maternal nutrients are supplied by the epithelial walls amphibian embryos enhances respiratory capabilities.
of the oviduct in viviparous Salamandra. In S. atra only Three pairs of external gills develop in salamanders and
1 or 2 eggs in each oviduct are fertilized; another 20 to caecilians. Among caecilians, the gills are triradiate, elon-
30 eggs degenerate into a mass of yolk, which is ingested gate, and plumose in groups exhibiting diverse repro-
by the developing fetuses after their own yolk reserves ductive modes—oviparity, ovoviviparity, and viviparity—
are exhausted; subsequently the fetuses are nourished but they are expended sheets in typhlonecüds (M. Wake,
by secretions from the oviducal walls (Wunderer, 1910; 1969) (Fig. 5-6).
Vilter and Vilter, 1960, 1964). Likewise, maternal nu- In most species of salamanders that develop in ponds,
trients are supplied via epithelial secretions in the oviducts the gills of the larvae have moderately long fimbriae and
by the viviparous frog Nectophrynoides occidentalis (Vil- a general bushy appearance. The gills are more robust
ter and Lugand, 1959; Xavier, 1973); fetuses have fine and have shorter fimbriae in those that develop in streams;
papillae around the mouth, but their funcüon in feeding, however, prior to hatching the gills of all aquatic sala-
if any, is unknown (Lamotte and Xavier, 1972). manders have only small fimbriae. Two different kinds
Caloric Utilization has been calculated for few species. of gills are present in the encapsulated larvae of terrestrial
From data on two species of anurans and two of sala- plethodontids undergoing direct development. In most
manders (Table 5-1), it seems evident that far more en- plethodontids the gilí rami are fused and the fibriae are
ergy is required to produce a larger hatchling than a smaller moderately long—the "staghorn" type of gilí; there is
one and that this requires considerably more time. Thus, variation in the number and lengths of the fimbriae (Vial,
increased amounts of energy are required simply to 1968; McDiarmid and Worthington, 1970), and the fim-
LIFE HISTORY
118

Figure 5-6. Gills of fetal caecilians. (Left)

Triradiate gills of Dermophís mexicanas. (Right)
Sheetlike gills of Typhlonectes compressicauda.

Figure 5-7. Gills of embryos of

terrestrial plethodontid salamanders.
A. Staghorn type in Pseudoeurycea
nigromaculata (McDiarmid and
Worthington, 1970). B. Elongate type
¡n Batrachoseps pacificas (J. Davis,
1952). C. Leaf type in Ensatina
eschscholtei (Stebbins, 1954).
Redrawn from sources cited; not to
scale.

briae are absent on fairly long rami in Batrachoseps at- and branched, and the tadpoles hang from the surface
tenuatus and B. pacificus (Emmel, 1924; J. Davis, 1952). of the water with their gills outspread untíl Stage 24,
However, in Aneides lugubris, Hydromantes shastae, and when the gills are reduced and the operculum closes.
Ensatina eschscholtzi the gills are flattened and leaflike External gills persist for a while after hatching in some
(Ritter and L. Miller, 1899; Gorman, 1956) (Fig. 5-7), species, the eggs of which develop in foam nests, such
whereas those of Aneides aeneus are intermedíate be- as Physa/aemus pustulosas (Noble 1927b) and Polype-
tween the staghorn and leaf types (Bishop, 1943). No dates leucomystax (Alcalá and W. Brown, 1956). Exter-
environmental or developmental factors seem to be cor- nal gills are especially well developed in embryos of some
related with these different types of gills in terrestrial eggs species that have eggs attached to vegetation over water,
of plethodontid salamanders. The gills of the viviparous such as Phyllomedusa (Pyburn, 1980a) and Centróle-
species of Salamandra have numerous and very long nella (Noble, 1927b; P. Starrett, 1960), but external gills
fimbriae (Gasche, 1939), presumably as an adaptatíon are absent from embryos in the arboreal eggs of Mantí-
to obtain oxygen in the oviducts. dacty/us líber (Blommers-Schlosser, 1975a).
Compared with other amphibians, extemal gills are In the egg-brooding hylid frogs, the eggs undergo di-
poorly developed in anuran embryos, but the larvae do rect development on the dorsum of the female or in a
have well-developed internal gills. With the exception of dorsal pouch; in some species carrying eggs in a pouch,
the egg-brooding hylid frogs, externa! gills are transitory, hatching occurs at a larval stage. The developing em-
if present at all, and usually do not persist after hatching. bryos of all seven genera are characterized by extensive
However, tadpoles of gladiator frogs of the Hyla boans bell-shaped gills that partially or completely envelop the
group have large filamentous gills (Noble, 1927b). The embryo and yolk sac. These gills are associated with only
gills develop soon after hatching (Stage 17) in Hyla ro- the first gilí arch in F/ectonotus and Cryptobatrachus, which
senbergi (Kluge, 1981); by Stage 19 the gills are large have only one pair of gills partially covering the embryo,
 Eggs and Development
or with the first and second gilí arches in Fritziana, Hem- accomplished by gaseous exchange between the embry-
iphractus, and Stefania, which have two pairs of gills that onic gills and vascularized maternal tissue.
cocnpletely envelop the embryo in all but Fritziana (del In some other anurans having direct development of
Rno and Escobar, 1981). Only one pair of gills is present terrestrial eggs, respiration presumably is enhanced by
TI Gastrotheca andAmphignathodon, but these have two the development of vascularized tissue other than gills.
pairs of stalks; the large single gilí apparently is the result The tail is greatly expanded and pressed against the vi-
oí fusión of two pairs (Fig. 5-8). telline membrane in the Papuan microhylid Phrynoman-
In aquatíc frogs of the genus Pipa, eggs are imbedded tis robusta (Méhely, 1901) and in many species of
in the dorsal skin of the female; small gills are present in Eleutherodactylus (Fig. 5-9), includingE. optatus (Noble,
«mbryonic P. carvalhoi (Weygoldt, 1976b). In that spe- 1927b), nubicola (Lynn, 1942), guentheri and nasutus
cies the implantation of the eggs involves extensive re- (Lynn and B. Lutz, 1946a, b), and johnstonei (Lamotte
organizaüon of the epidermis and dermis of the female's and Lescure, 1977). The tail develops into a thin mem-
dorsum. The egg chambers are well supplied with cap- brane that almost completely envelops the embryo in
Baries, and the single jelly capsule of the egg adheres to Hylactophryne augusti (Jameson, 1950; Valett and
tte wall of the chamber. The lining of the pouches of Jameson, 1961). However, in other species of Eleuth-
brooding females of egg-brooding hylids is highly vas- erodactylus (e.g., E. p/anirostris, Goin, 1947) the tail is
cularized and also has extensions of vascularized üssue not expanded. In most species of Eleutherodactylus that
between the eggs (del Pino et al., 1975). The gills of the have been studied, extemal gills are absent, but they do
embryos are separated from the maternal tissue by a thin appear for a brief period of time in at least three species—
jefly capsule. It is evident that embryonic respiration is E. inoptatus, johnstonei, and poríoricensis; in the last
species the gills are associated with the third gilí arch
(Gitlin, 1944). The gills presumably function in respira-
tion before the highly vascularized caudal tissue expands
and assumes this function.
Externa! gills are absent or transitory in other frogs
having direct development. The tail is vascularized but
not greatly expanded in embryos of frogs such as Leio-
pelma (E. Stephenson and N. Stephenson, 1957), the
microhylid Myersiella microps (Izecksohn et al., 1971),
and the ranid Anhydrophryne mttrayi (Wager, 1965).
Platymantine ranids of the genera Discodeles and Pla-
tymantis have direct development of terrestrial eggs. Their
embryos have vascularized, thin-walled, lateral, abdom-
inal sacs that presumably function in respiration (Fig. 5-
9); in these embryos the tail is small and external gills
are absent (Boulenger, 1886; Atoda, 1950; Alcalá, 1962).
Among the viviparous species of Nectophrynoides, the
tail is relatively long and thin but well vascularized (La-
motte and Lescure, 1977), and it may serve respiratory
functions. The tail in the ovoviviparous Eleutherodactylus
jasperi is greatly expanded (M. Wake, 1978).
Figure 5-8. Gills of an embryo of the egg-brooding hylid frog In summary, embryonic respiration in both aquatic and
Gastrotheca cantuta. terrestrial eggs of caecilians and salamanders and vivi-

Figure 5-9. Respiratory structures of embryos

of anurans having direct development of
terrestrial eggs. (Left) Expanded vascularized tail
in Toirwdactylus nítidas. (Right) Expanded
abdominal folds in Platymantis guentheri.
LIFE HISTORY
parous species of caecilians is accomplished by external respectively, is 0.172, 0.046, and 0.046 mg per 100 eggs
gills. Other tissues (tail or abdominal walls) perform this per day at the neurula stage, but increases to 0.721,
function in the embryos of some terrestrial anurans, 0.525, and 0.242 mg per 100 eggs per day just before
whereas gills are the primary respiratory organs in em- hatching (Munroe, 1953). However, ureotelism may be
bryos of some other anurans. The smaller total surface common in terrestrial and arboreal eggs, for which large
área of gills of embryonic salamanders as compared with quantities of water are not available for the ready disposal
those in most aquatíc larval salamanders suggests that of ammonia. Urea accounts for as much as 86% of the
less oxygen is consumed per unit time as embryos than nitrogenous wastes in the terrestrial eggs of Geocrinia
as active free-swimming larvae. However, no comparable uictoriana (A. Martin and A. Cooper, 1972). Further-
measurements of respiratory rates of eggs of diverse de- more, urea accumulates at a much faster rate than am-
velopmental modes and corresponding larvae are avail- monia in the terrestrial foam nests of Leptodacty/us a/-
able. Gilí growth in embryos of Rana pipiens and R. bi/abris and L. bu/onius (Candelas and Gómez, 1963;
temporaria can be suppressed by elevated oxygen ten- Shoemaker and McClanahan, 1973). The accumulation
sión and promoted by high carbón dioxide pressure of whitish crystalline deposits within the egg capsules and
(Lóvtrup and Pigon, 1969). on the tail during late intracapsular development in Ba-
The rate of oxygen consumption is known to increase trachyla taeniata suggests the possibility that these em-
during intracapsular development in some amphibians: bryos might be excreting uric acid (Cei and Capurro,
Bu/o (Wills, 1936), Rana temporaria (Brachet, 1934), 1958).
Ambysfoma (Hopkins and Handford, 1943), Taricha Although relative concentrations of ammonia and urea
(Connon, 1947), Ascaphus (H. Brown, 1977), and vari- have not been measured in arboreal eggs, such as those
ous species of Japanese anurans (Kuramoto, 1975). This of Phyí/omedusa hypocondria/is, probably the majority
increase occurs in two phases, at pre- and postneurula- of nitrogenous wastes is in the form of urea. Embryos of
tion, with a plateau during early stages of neurulation in such frogs have a limited external water supply—the egg-
Rana (Barth and Barth, 1954) and later stages of neu- less capsules. As noted by Pyburn (1980a), in early de-
rulation in Ambystoma (Ltóvtrup and Werdinius, 1957). velopmental stages, the increasing osmotic pressure of
Except for the earliest developmental stages, the embryos the perivitelline fluid causes water to diffuse from the
of anurans have higher levéis of oxygen consumption adjacent eggless capsules into the perivitelline space, di-
and more rapid rates of increase than do salamanders luting the concentration of nitrogenous wastes. Because
(Atlas, 1938; Fischer and Hartwig, 1938). However, the of the limited supply of water in the eggless capsules,
total amount of oxygen consumed during neurulation is eventually the rate of dilution becomes less than the rate
about the same even though they respire at different rates of waste concentration in the perivitelline fluid. Accu-
(Spirito, 1939), because neurulation is a longer process mulation of metabolites in late embryonic stages is evi-
in species having comparatively low respiratory rates than dent by the amber color of the perivitelline fluid.
in those having faster rates. Interspecifically, there is a A green alga (Ch/amydomonos sp.) occurs symbioti-
positive correlation between rapid development and high cally in the perivitelline fluid of the eggs of Ambystoma
rates of oxygen consumption (Connon, 1947). Within graci/e (Goff and Stein, 1978). The alga removes am-
species, larger ova consume more oxygen at a given stage monia from the perivitelline fluid and stores the excess
than do smaller ones (Barth and Barth, 1954), but this nitrogen as membrane-bound proteinaceous bodies; this
correlation does not hold between species (Connon, 1947). symbiotic relationship apparently affects the rate of de-
The large ova of Ascaphus truei have extremely low rates velopment and survivorship, which is higher in the pres-
of oxygen consumption; this is related to the low tem- ence of the alga than in its absence.
peratures at which they develop and suggests the pres-
ence of a large amount of inactive cytoplasm in the de- Temperatura and Development
veloping embryos (H. Brown, 1977). Various environmental factors influence the development
of amphibian embryos. These will develop normally only
Nitrogenous Wastes. Amphibian embryos and lar- within certain limits of salinity and pH (see Dobrowolski,
vae generally excrete nitrogenous wastes in the form of 1971, for review). The most extensive work has been
ammonia (J. Balinsky, 1970). In an aquatic environment with the relationship of temperature and development
large quantities of toxic ammonia can be diluted by con- The pioneering quantitative work of Lillie and Knowlton
tinual diffusion of water into the perivitelline fluid. Thus, (1897) demonstrated the negative correlation between
although aquatic amphibian eggs are primarily ammon- developmental time and temperature, within the thermal
otelic, small amounts of urea are produced by aquatic limits of the eggs, in amphibians. Subsequent work, prin-
eggs, and the total amount of ammonia and urea in- cipally initiated by Moore (1939), showed a correlation
creases during development. For example, urea amounts between breeding habits and geographic distribution on
to 10 to 20% of the total amount of excretory producís one hand and temperature tolerances and rates of em-
in Rana temporaria, Bu/o bu/o, and Xenopus laevis. The bryonic development on the other. Experiments on Rana
amount of urea produced by eggs of these three species, pipiens and R. temporaria by Atlas (1935) and Svinkin
 Eggs and Developmen
IJ962), respectívely, demonstrated that later embryonic 12
tfages have broader temperature tolerances than do ear- 10O-
fcr stages.
Bélehrádek (1957) noted that viscosity varíes with
fcmperature, as does the developmental rate, but reac-
ton rates do not; therefore, he concluded that biochem-
icai rates in intact organisms are diffusion-restricted. Data
oc embryos of Rana pipiens suggest that shifts in tem-
perature responses may be related to changes in viscosity
fufcLaren, 1965). Salthe and Mecham (1974) attempted
to show that as ovum size, altitude, or latitude increases,
±>e rate of development at a given temperature increases.
However, interspecific comparisons between ovum size
and developmental rate are the inverse (see Chapter 2).
Most^amphibian embryos that have been studied de-
vriop normally with a temperature range of about 15 to
20FC; the upper and lower lirnits of this range are species-
^iccific or in some cases are variable between intraspe-
ti&c populations living in different environmental re-
ymes. At temperatures near the upper limit, develop-
snent proceeds much faster than at temperatures near
fie lower limit, and this temperature-dependent accel-
eration is the same for all embryonic stages. Therefore,
K. Bachmann (1969) concluded that within the normal
tange of temperatures for a species or population, a gen-
ecal rate of development can be determined as the in-
wrse of the time interval between any two develop-
mental stages. In view of the complex timing relations of .00-
taductive processes in amphibian embryology, the tem-
0 10 20 30
perature independence of the relative timing of devel-
opmental progress appears to be an important specific Temperature (°C)
or populational adaptive feature. Furthermore, at tem- Figure 5-10. Temperature relationships of embryonic development
peratures only a little above or below the range of 100% in Bu/o valliceps. A. Máximum and mean survival of batches of
eggs at different temperatures. B. Rate of development (reciproca!
normal development, the relative timing begins to vary, of time in hours between first cleavage and gilí circulation x 103)
resulting in abnormal embryos, and at extreme temper- to Stage 20 (gilí circulation) at different temperatures. Note the
correspondence between 100% possible survival in A and the linear
atures no development at all. For example, at 20 to 33°C part of the rate curve in B. See text for definitions of T0 and (T0 +
nearly all embryos of Bu/o valliceps develop normally, 10). Adapted from K. Bachmann (1969); data from Volpe (1957a).
but normal gastrulation does not occur at 15 or 36°C
(Volpe, 1959a) (Fig. 5-10A). Temperature ranges for
normal development vary among species. However, within the valúes are between 20 and 25°C for most warm-
Ihat range of temperature the overall rate of development adapted species (K. Bachmann, 1969).
is the only feature that varíes with temperature. K. Bach- Comparison of embryonic developmental rates inde-
mann (1969) suggested that developmental rate is a lin- pendent of temperature necessitates the measurement of
ear function of temperature throughout the range of 100% the product of the time interval between two comparable
survival (Fig. 5-10B), but McLaren and Cooley (1972) stages. Usually these are the two-celled stage (Stage 3 of
questioned the linearity of the relationship. R. Harrison, 1969, for Ambystoma, and Gosner, 1960,
The intercept of the rate-temperature line with the tem- for anurans) and the closure of the neural tube (Stage
perature axis (T0) usually lies below the range in which 21 of R. Harrison, 1969, for Ambystoma; Stage 16 of
normal development occurs. However, the temperature Gosner, 1960, for anurans). Using (16) as a standard for
10°C above T0 not only lies near the middle of the adap- completion of neural tube formation, K. Bachmann (1969)
tive temperature range of every species but also is the measured the progress of development as
temperature at which the temperature coefficient (Q10) (16) = At(16)(T-T0)
of the development rate is equal to 2. Therefore, (T0 +
10) is a constant relating the temperature effect on de- where AD(16) is the developmental interval between the
velopmental rate to the temperature range to which the two-celled stage and closure of the neurula, At(16) is the
embryos are adapted. Cold-adapted amphibians typically time interval between the two stages, T is the develop-
have valúes of (T0 + 10) between 10 and 15°C, whereas mental temperature, and T0 is a constant.
LIFE HISTORY
Comparison of data on various amphibians reveáis that developmental rates at the same temperatures. For ex-
adaptive temperaturas (T0 + 10) vary from 10 to 27°C, ample, embryos of Ambystoma gracile require about half
and that the relatíve rates are highly variable (Table as much time to reach the stage of gilí circulation as do
5-2); the temperature tolerances are measured from first those of A. tigrinum; A. jeffersonianum develops even
cleavage at constant temperatures. The relative devel- faster (Table 5-3). Studies on cold-adapted species reveal
opmental rates of Bu/o in warm waters is much faster similar ranges of thermal tolerances but notably different
than Rana in cold waters or than aquatic salamanders. rates of development at constant temperatures. For ex-
In comparison with anurans, most salamanders have much ample, three amphibians breeding in the same pond in
narrower ranges of adaptive temperatures; however, extreme northwestern Washington, have embryonic tem-
Ambystoma gracile has developmental temperature tol- perature tolerances of 4-21°C (Rana aurora], 5-22.5°C
erances of 5 to 22.5°C (H. Brown, 1976a). Furthermore, (Ambystoma gracile), and 6-28°C (Hyla regula), but at
salamander embryos require about half again as much 10°C gilí circulation is reached in 16 and 19 days re-
time to reach a given stage of development as do anu- spectively in H. regula and R. aurora but not until 36
rans. These generalizations are based on data on rela- days in A. gracile (H. Brown, 1976a). The embryos of
tively few species, all of which have aquatic eggs and Ascaphus truei in streams in the same área tolérate tem-
larvae. Comparable kinds of data are needed on sala- peratures of only 5-18°C and require 27 days at 10°C
manders and anurans having direct development and to attain gilí circulation (H. Brown, 1975a). The ranges
anurans having other diverse reproductive modes. of temperature tolerances of these cold-adapted species
Still, it is obvious that different species have different (13.5-17.5°C) is slightly more than the range

Table 5-2. Valúes for the Adaptive Temperature (T0 + 10) and the Relaüve Developmental Time from the Two-celled Stage to Closure of the
Neurula for Various Amphibians"
r0 + 10 AD(16)
Species (°C) (°C x hours) Reference
Salamanders
Cynops pyrrhogoster 17.2 1287 K. Bachmann (1969)
Notophthalmus viridescens 17.3 1092 K. Bachmann (1969)
Triturus alpestrís 15.0 1222 Knight (1938)
Ambystoma maculatum 15.8 1335 K. Bachmann (1969)
Ambystoma mexicanum 18.2 861 K. Bachmann (1969)
Ambystoma tigrinum 17.8 822 Moore (1939)
Ambystoma íigrinum 19.0 860 Tamini (1947)
Proteus anguineus 18.0 (5000)6 Briegleb (1962b)

Anurans
Ascophus truei 14.4 1817 H. Brown (1975a)
Xenopus laeuis 20.5 252 Nieuwkoop and Faber (1956)
Scaphiopus hammondii 23.3 183 H. Brown (1967b)
Scaphiopus mu/tip/icatus 24.5 137 H. Brown (1967b)
Bufo americanus 24.2 250 Volpe (1953)
Bufo bufo bufo 15.5 912 Douglas (1948)
Bufo bufo japonicus 10.2 1650 Hasegawa (1960)
Bufo terrestris 24.5 (200)" Volpe (1953)
Bufo valliceps 24.8 (200)" Volpe (1957a)
Bufo woodhousii fowleri 24.9 250 Volpe (1953)
Bufo woodhousii woodhousii 25.0 (250)b Volpe (1953)
Hyla arbórea 19.2 556 Tamini (1957)
Rana berlandieri (Veracruz) 22.3 379 Ruibal (1955)
Rana berlandieri (Texas) 21.6 438 Moore (1949)
Rana catesbeiana 24.3 357 Moore (1939)
Rana c/amitans 21.0 475 Moore (1939)
Rana escu/enta (Germany) 18.0 602 Hertwig (1889)
Rana escu/enta (Italy) 21.6 430 Tamini (1947)
Rana escu/enta (England) 24.0 350 Douglas (1948)
Rana pa/ustn's 19.0 703 Moore (1939)
Rana pipiens (New Jersey) 20.0 500 Moore (1949)
Rana pipiens (Wisconsin) 20.8 451 Moore (1949)
Rana pipiens complex (Costa Rica) 22.0 500 Volpe (1957b)
Rana septentriona/is 22.4 525 Moore (1952)
Rana shenocephala 23.0 344 Moore (1949)
"Extracted from K. Bachmann (1969).
blnterpolated data.
 Eggs and Development
Tibie 5-3. Comparative Rates of Embryonic Development of Rve Species of Ambystoma to Different 123
Developmental Stages from First Cleavage*

Time in hours to
Muscular Heart- Gilí
Species and temperature Castróla response beat circnlatíon
A jeffersonianum (19.9°C) 18 83 103 120
A tigrinum (19.9°C) 24 105 122 146
A maculatum (20°C) 45 165 175 195
A mexicanum (18°C) 52 155 165 197
A groóle (20°C) 36 262 283 305
•Adapted from H. Brown (1976a).

TaMe 5-4. Comparative Rates of Embryonic Development of Six Species of Anurans in a Desert Región in
Southeastem Arizona at Different Temperaturas"'1'
Constant temperature Range of
Species 21°C 26°C 32°C
tolerance (°C)

Bu/o cognutus 86 43 25.5 16.0-33.5

Bufo debilis 88 39 24 18.2-33.8
Bufo punctatus 76 40.5 22.5 16.0-33.0
Scaphiopus bombifrons 41 27 19.5 13.0-31.5
Scaphiopus couchii 57.5 25 16.5 15.5-34.0
Scaphiopus multiplicatus 42 29 28 15.6-32.5
•ftdapted from Zweifel (1968b).
Time is given in hours to reach gilí circulation.

(17.0-19.5°C) of six species of anurans studied in an freezing temperatures is unknown. Likewise, little infor-
área of sympatry is southeastem Arizona {Zweifel, 1968b). maüon is available on the tolerance levéis of embryos
The lowest temperature at which normal development exposed to high temperatures for varying periods of time
occurred was in Scaphiopus bombifrons (13.5°C), whereas or on tolerance changes during ontogeny. The only thor-
Bu/o debilis required temperatures of 18.2°C. The high- ough experiments of this type have dealt with North
est temperatures tolerated were 33.8 and 34.0°C by B. American (H. Brown, 1967a; Zweifel, 1977) and Japa-
debilis and S. couchii, respecüvely, whereas S. bombi- nese (Muto and Kawai, 1960; Kuramoto, 1978) anurans.
frons could tolérate temperatures of only 31.5°C. Within Among most species studied, the máximum temperature
the ranges of temperature tolerances the rates of devel- tolerated is inversely related to the duration of exposure
opment were notably faster at higher temperatures (Table (Table 5-5). Bu/o cognatus is an exception in that the
54). duration of exposure had no obvious effect on máximum
No geographic variatíon in temperature tolerances is tolerance, which was less than 40°C (Zweifel, 1977); also,
evident in such widely distributed species as Rana cates- exposure of embryos of R. limnocharís to temperatures
beiana, clamitans, sylvatica, or Scaphiopus couchii (Moore, of 43°C for 2 and 6 hours had no effects on máximum
1939,1942; Herreid and Kinney, 1967; Zweifel, 1968b). tolerance (Kuramoto, 1978). Embryos of all species stud-
But geographic variation is known in at least three species ied increase their temperature tolerances as they grow; a
of anurans—Bu/o amen'canus, B. uioodhousii, and Hyla marked increase takes place early in development during
regilla (Volpe, 1953; H. Brown, 1975b)—and two of sal- the first several cleavages. Rana sylvatica, a cold-adapted
amanders—Ambystoma maculatum and A. macrodac- species, does not attain máximum tolerance until gastru-
tylum (DuShane and C. Hutchinson, 1944; J. Anderson, lation is complete, or nearly so; Scaphiopus couchii, which
1967). Apparent geographic variation in Scaphiopus develops in warm water, achieves more than 90% of its
hammondii (H. Brown, 1967b) reflects the inclusión of total tolerance before the beginning of gastrulation (Fig.
two species (H. Brown, 1976b). Geographic variation in 5-11). Experiments with American anurans were termi-
Rana pipiens (Moore, 1949) is explained, in part, by the nated at Stage 20, but those on Japanese anurans by
inclusión of several sibling species (Pace, 1974). Kuramoto (1978) were conttnued until Stage 25; im-
In nature, developing eggs of Rana aurora are known mediately after hatching the temperature tolerances are
to survive short exposures to freeáng temperatures (Storm, much lower than in stages 11-20.
1960), but the differential survival of different develop- Amphibians are adapted to temperature regimes of the
mental stages exposed to varying duraüons of low or breeding habitat in two ways. One is a behavioral ad-
LIFE HISTORY
124 Table 5-5. Máximum Temperatures (°C) Tolerated by Anuran Embryos for Different Periods of Exposure"'1"
Species Base level 2 honra 4 honra 6 honra 10 honra
Rana sylvatica 24.0 34.6 (10.6) 33.7 (9.2) 32.9 (8.9) 32.6 (8.6)
Hyla regula 29.6 38.0 (8.4)
Rana chiricahuensis 31.5 37.7 (6.2) 37.6 (6.1) 37.5 (6.0) 36.8 (5.3)
Scaphiopus bombifrons 32.5 40.0 (7.5) 39.2 (6.7) 39.2 (6.7) 39.2 (6.7)
Scaphiopus muttiplicatus 32.5 40.4 (7.9) 40.0 (7.5) 39.0 (6.5)
Scaphiopus couchii 34.0 40.3 (6.3) 39.8 (5.8) 39.8 (5.8) 39.5 (5.5)
Bufo cognatus 33.5 >40.5 (>7.0) >40.5 (>7.0) >40.5 (>7.0)
"Adapted from Zweifel (1977).
bFigures in parentheses represen! increase over base-level tolerance.

be physiological limitations that prevent early embryos

40 from being adapted to both extremely cold and ex-
tremely warm temperatures. "Given a restricted range of
38
temperature tolerance at the beginning of life and having
g36 no way of actively avoiding detrimental temperatures
£
-3 34
should they occur, the obvious adaptive change is for the
S. 32 embryo to widen its range of tolerance as it grows" (Zweifel,
1977:14). Rapid changes in tolerances may be an adap-
|30- 1. Bufo cognatus tation to shorten the period in which an embryo is sen-
& 28- 2. Scaphiopus couchi sitive to high temperatures. For example, the temperature
3. Scaphiopus bombifrons
26-
of the water in shallow ponds is within the range of tol-
4. Rana chiricahuensis
5. Rana sylvatica erance of early embryos of Scaphiopus when they de-
24- posit their eggs at night. By midday the temperature of
17 the water frequently is above the level of tolerance of
Stage of Development early embryos, but by that time the rapidly developing
embryos have reached a point where their tolerance in-
Figure 5-11. Ontogenetic changes in 2-hour temperature corporales the higher temperatures (Zweifel, 1968b, 1977).
tolerances in embryos of five species of anurans. Stages of
development follow Gosner (1960); the developmental axis is Thus, the critical thermal máxima, rate of change of tol-
adjusted to be approximately linear with respect to time. Adapted erance, and developmental rate may have been modified
from Zweifel (1977).
by selective pressures directly relating to environmental
temperature.
The mechanism of embryonic temperature tolerance
justment; the time and/or place of breeding are governed is unknown. Genetic control has been questioned, be-
by temperatures suitable for embryonic development. cause the early temperature tolerance of hybrid embryos
Thus, there is a cióse correspondence between temper- is not intermedíate between the parents but maternal in
ature tolerances and the temperatures encountered in the nature. For example, hybrid embryos of Bufo americanus
breeding sites (Kobayashi, 1963; Ballinger and Mc- X B. woodhousii are maternal in their temperature tol-
Kinney, 1966). Also, temporal differences prevalí at given erance (Volpe, 1952). Kuramoto (1978) suggested the
localities; temperature tolerances of species breeding later participation of cytoplasmic factors in determining the level
in the summer in central Texas are higher than those of of temperature tolerance of early embryos; a relatively
species breeding earlier in cooler water at the same lo- sharp increase of tolerance during early cleavage stages
calities (Hubbs et al., 1963). may be the result of progressive partitioning of cytoplasm
A second adaptation involves modifications of embry- or may be mediated by maternal messenger RNA tran-
onic temperature responses. If a species is sufficiently scribed in oogénesis. Some of the maternal contribution
conservativo in its selection of times and places of breed- to the level of tolerance may be provided by the muco-
ing, or if the habitat is extrernely stenothermic, there is polysaccharide capsules. Certainly the number, thick-
no need for embryonic adaptation to a broad range of ness, and viscosity of the capsules are important in pro-
temperatures. For example, populations of the Rana pi- viding the early embryo with some protection from rapid
piens complex living in environments with relatively little changes in temperature.
fluctuation in temperature during the year have relatively
narrow embryonic temperature ranges compared with Patterns of Development
populations living in environments with great fluctuations Although much has been written about amphibian de-
in temperature (Ruibal, 1962). Such conservativeness re- velopment, most of these investigations have not been
stricts the successful breeding of a species should the concerned with the evolutionary or ecological aspects of
environment change. On the other hand, there seem to development. This section discusses briefly the pattems
 Eggs and Developmen
of development that seem to be evident on the basis of Beginning at the neurula stage, amphibian embryos
comparative embryology. Details of the development of are ciliated. The motíons of the cilia keep the embryo
Ihe skeletal system in posthatching larvae are given in constantly rotatíng in the perivitelline fluid. There is some
Qiapter 6. evidence that prolonged contact of the embryo with the
vitelline membrane results in cytolysis; motion of the per-
Eariy Development. Cleavage in amphibian eggs is ivitelline fluid may aid in the dispersa! of oxygen prior to
hdoblastic and unequal; in large ova, many divisions the development of specialized respiratory structures
may occur on the animal hemisphere before the first (Bayley, 1950).
deaves through the vegetal pole. Ichthyophis g/uíinosus
is the only caecilian for which cleavage has been de- Operculum Development. The operculum, that
soibed (P. Sarasin and F. Sarasin, 1887-90). In that sheath of tissue covering the branchial chambers, arises
species cleavage is nearly meroblastic, that is, as a result from the hyoid arch anterior to the first branchial slit. The
of incomplete cleavage the egg is divided into numerous posterior growth of the paired opercula results in the
sepárate blastomeres and a residual multinucleate mass eventual covering of the branchial chambers and fusión
of cytoplasm. Cleavage through the blástula stage is es- of the bilateral extensions midventrally. In salamanders
sentially idéntica! among those amphibians that have been and caecilians, gilí slits persist and externa! gills protrude
studied. The blastocoel occupies a relaüvely small área from the posterolateral margins of the opercular sheaths,
near the animal pole in larger ova. while internally a single, median branchial chamber ex-
Differences in gastrulation seem to be associated with ists.
Ihe amount of yolk. In most salamanders and anurans The development of the operculum in anurans is more
the entire yolk is covered as the blastopore closes, but in complex, and the differences in opercular development
caecilians the blastopore becomes circular while the yolk among anurans are associated with the buccal pump
still is mostly uncovered. In this way the blastopore be- mechanism and the interna! gills. The covering of the gills
comes surrounded by the blastodisc on the upper surface necessitates the development of an outlet for water
of the partly divided egg. Also, a blastodisc is formed in pumped over the gills. This outlet, the spiracle, is single
the marsupial frog, Gastrotheca riobambae (Elinson and in all but the pipoid frogs, in which it and the branchial
del Pino, 1982). chambers are paired. In some embryos having direct de-
In embryos of anurans and salamanders that develop velopment, an operculum and branchial chambers never
from large-yolked eggs, development takes place on the develop (e.g., Eleutherodactylus; Lynn, 1942), but in
surface of the animal hemisphere, and the bulk of the otheers (e.g., Leiopelma) an operculum develops but does
yolk is not incorporated into the gut but instead forms a not cover the forelimbs (N. Stephenson, 1951b).
tónd of yolk sac. In most eggs having small amounts of
yolk, as is characteristic of aquatíc eggs, the yolk is in- Gilí Development. Embryos of caecilians and sala-
corporated into the gut at early stages. Notable excep- manders develop three pairs of external gills (Branchial
tions are embryos developing in aquatíc (Physalaemus arches III, IV, V), whereas anuran embryos lack gills or
pustulosas, Noble, 1927b) and arboreal (Rhacophorus have as many as three pairs of external gills. Usually only
schiegeli, Ichikawa, 1931; Chiromantis petersi, Cherchi, two pairs of gills appear in anurans (Branchial arches III
1958) foam nests and those developing on vegetation and IV). In most frogs hatching occurs after the devel-
above water—phyllomedusine hylids and centrolenids. opment of the gills, but the embryos of some others (e.g.,
The eggs of these frogs are reasonably small, but their Xenopus, Discoglossus, some Scaphiopus, and some Bufo)
development is like those of telolecithal eggs. hatch before the gills develop. In any case, gills are tran-
At the tail-bud stage, caecilians and salamanders have sient in anurans having aquatic larvae. Three pairs of gills
relatively long necks incorporattng the gilí plates and pro- develop in the African bufonid Schismaderma carens
jecting forward from the yolk mass, but have only a short (B. Balinsky, 1960). Gills develop only from the third
tail bud. In anurans, the gilí píate región is above the yolk branchial arch in some egg-brooding hylid frogs and from
mass with only a small portíon of the head projectíng Branchial arches III and IV in other species. Gills are
beyond the yolk, but a relatively long tail bud is present. absent in embryos of many frogs that have direct devel-
These differences, first pointed out by Kerr (1919), are opment of terrestrial eggs, but externa! gills rnay be present
generally consisten! regardless of ovum size or subse- briefly in some species of Eleutherodactylus. Also, both
quent mode of development. The relaüve length and internal and external gills are absent in the viviparous
freedom of the gilí píate región may be indicativo of the Nectophrynoides occidentalis (Larnotte and Xavier,
comparatívely greater degree of development of external 1972b).
gills in caecilians and salamanders as contrasted with The absence of external gills in aquatic feeding stages
anurans. However, the neck región is exceedingly long of anuran larvae is associated with the presence of filter
in embryos of Eleutherodactylus (Lynn, 1942; Lynn and feeding and the buccal-pump mechanism in tadpoles, in
B. Lutz, 1946a, 1946b). During the development of these which water is pumped over well-developed internal gills.
terrestrial eggs, interna! gills are absent, and external gills Internal gills are developed on all four gilí arches in prim-
are absent or poorly developed and transitory. itive frogs having aquatic larvae; no patterns are evident
LIFE HISTORY
126 in the absence of gills on certain arenes in other anurans The ecological correlatos of limb development in sal-
(Sokol, 1975). Moreover, the presence of internal gills in amanders also are influenced by the amount of yolk
anurans and their absence in salamanders are rnostly a available to the developing embryos (Salthe and Me-
difference in posiüon. There is developmental (E. Ger- cham, 1974). Salamander larvae hatching from small eggs
hardt, 1932) and morphological (Schmalhausen, 1968) have only the forelimbs present and continué their de-
evidence that the internal gills in anurans are merely ven- velopment and differentiation as feeding larvae. Stream-
tral extensions of the external gills. The latter do not de- inhabiting larvae require limbs to maintain their position
velop at all or disappear soon after hatching in frogs, in in flowing water; at hatching these larvae have hindlimbs,
contrast to aquatic salamander larvae. and the energy for the development is supplied by the
larger amount of yolk in their eggs. Terrestrial pletho-
Limb Development. Vestigial limb buds appear in dontids, which must be capable of locomotion on land
¡chthyophis g/utinosus (P. Sarasin and F. Sarasin, upon hatching, have fully developed limbs, and all of the
1887-90) but not in other oviparous caecilians that have energy for their development is supplied by yolk.
been studied: Hypogeophis (Brauer, 1899) and Siphon- The same ecological and energy correlatos apply to
ops (Goeldi, 1899). anurans. Tadpoles that hatch in an early stage of devel-
In embryos of aquatic salamanders there is a definite opment live in still water and obtain energy from the
anteroposterior wave of limb development, and the digits environment for their continued development, whereas
appear sequentially on both sets of limbs. In species de- those that develop directly into terrestrial froglets obtain
veloping in still water, only the forelimbs develop before all of the energy for their development from large quan-
hatching, and these have partially undifferentiated digits. tities of yolk.
Differential timing of development of forelimbs and hind-
limbs in embryos of stream-inhabiting salamanders is de- Balancers and Adhesive Organs. In pond-dwelling
creased. The hindlimb buds appear relatively sooner, and salamanders of the Hynobüdae, Salamandridae, and
more of the digits appear simultaneously on both sets of Ambystomatidae, ectodermal projections, known as bal-
limbs. At hatching most of these larvae have forelimbs ancers, develop from the mandibular arch shortly after
and hindlimbs with most of the digits developed. In pleth- the appearance of the forelimb buds. These rodlike struc-
odontid embryos undergoing direct development, the tures, one on each side of the head, contain nerves and
hindlimb buds appear almost simultaneously with the capillaries and produce a sticky, mucous secretion (Fig.
forelimbs, and all of the digits appear at the same time. 5-12). Balancers prevent early larvae from sinking into
In most anurans having free-swimming larvae, limbs the sediment and also help them to maintain their bal-
do not develop until after hatching. The hindlimb appears ance until the forelimbs develop. At that time the bal-
as a bud, as it does in salamanders, and undergoes growth ancers break off or gradually degenerate.
and differentiation externally, while the forelimb develops The adhesive organs (cement organs or suckers) in
within the branchial chamber, only to appear outside the anuran embryos and early larval stages also are ecto-
body during metamorphic climax. Among anurans hav- dermal in origin, but these structures are derived from
ing terrestrial eggs without a free-living larval stage, the the hyoid arch, rather than the mandibular arch.
forelimbs may develop externally and nearly at the same Morphological and histological studies of balancers and
time as the hind limbs, as in E/eutherodacty/us (Salthe adhesive organs led Lieberkind (1937) to conclude that
and Mecham, 1974), or they may develop simultane- they are not homologous.
ously, as in Leiopelma (N. Stephenson and de Beer, Adhesive organs develop at about the same time as
1951). However, hindlimbs appear before forelimbs in the tail bud. In discoglossoids and pipoids the organ is
the viviparous Nectophrynoides occidentaüs and the bipartite, but the two halves function as a single structure.
ovoviviparous N. tomieri (Lamotte and Xavier, 1972a, In Pelábales, it is Y-shaped. In all higher frogs, adhesive
1972b). organs are single median structures until the opercular
folds cióse; at this stage the adhesive organ is divided
into two parts (Fig. 5-12). The adhesive organ secretes
a sticky mucus, which may result in a threadlike conec-
tion between a recently hatched tadpole and the egg
capsule (Fig. 5-13), or the recently hatched tadpoles may
adhere to vegetation. By means of the adhesive organ,
a tadpole that hatches at an early developmental stage
may stabilize its position in the environment until its tail,
muscular coordination, and mouth have developed to
the point that the larva can swim and feed. Embryos that
Figure 5-12. Embryonic structures ¡n amphibians. (Left) Balancer have a long intracapsular development and hatch at later
in Pleurodeles waltl. (Right) Adhesive organ in Bu/o calamita. Both
structures develop in late embryos and degenerate shortly after stages may have transient adhesive organs. Once tad-
hatching. poles begin feeding, the adhesive organs degenerate. In
 Eggs and Development
rula stages are rapid, whereas successive larval stages
may be separated by several days or even weeks.
Normal stages in salamanders and anurans are quite
different after gastrulation, especially the timing of neu-
rulatíon and limb and gilí formation. Furthermore, there
is some variation within these groups.
In recent years, R. Harrison's (1969) numbered stages
of normal development in Ambystoma maculatum have
been considered the standard for salamanders, and Gos-
ner's (1960) generalized table is accepted as a standard
for anurans. These tables are basically applicable to taxa
that have aquatic eggs and larvae; interspecific compar-
isons can be made and differences noted readily.
ülustrations and brief descriptions of the standard stages
of salamander and anuran development follow.

Salamanders. This account is based on the stages of

development of Ambystoma maculatum (R. Harrison,
1969) (Figs. 5-14, 5-15); hours given in parentheses after
the stage number are for development at 20°C.

1. (0) Single cell; second polar body released.

2. (6.5) First cleavage; 2 blastomeres.
3. (8.0) Second cleavage; 4 blastomeres.
4. (9.5) Third cleavage; 8 blastomeres.
; 5-13. Function of adhesive glands in Xenopus laevis. (Left)
5. (11.0) Fourth cleavage; 16 blastomeres.
Ifatching tadpole leaving egg capsule attached to twig in water; a 6. (13.5) Fifth cleavage; 24 blastomeres by di-
Afead of mucus frorn the adhesive gland to the egg is obscured by visión of only those in animal hemisphere.
te tadpole. (Right) The same tadpole a few seconds later hanging
K a thread of mucus to the shrinking egg capsule. The tadpole 7. (17.5) Irregular cleavage into about 100 blas-
irmains in this suspended position until it has developed an tomeres.
efective tail and mouth. Redrawn from Bles (1905). 8. (22.0) Early blástula.
9. (29.0) Late blástula; animal hemisphere con-
sisting of several layers of cells.
10. (42.0) Invagination of dorsal lip of blastopore.
some frogs that have direct development of terrestrial 11. (58.0) Dorsal lip of blastopore expands into
eggs (e.g., Eleutherodactylus) adhesive organs never ap- semicircle.
pcar. 12. (65.0) Blastopore formed, surrounding yolk
plug; blastopore elevated to point of poste-
Normal Stages of Development rior axis of embryo.
The changing appearance of embryos, especially during 13. (72.0) Blastopore is narrow vertical opening;
organogénesis, necessitates a method of quantifying the neural keel on dorsal surface; body begins
progress of development. Tables of normal stages of de- to elongate.
velopment have been worked out for a number of spe- 14. (75.0) Dorsal flattening; neural píate forms.
cies (Table 5-6). Complete tables of development are 15. (80.0) Neural píate shield-shaped, bordered
necessary for accurate comparison of developmental stages by low neural folds.
in different organisms. Each stage must be identífied as 16. (84.0) Neural folds elevated.
to age at a given temperature; the stages then can be 17. (88.0) Neural folds further elevated; one pair
identified mostly by external features. During cleavage, of somites.
the stages are determined from the number and size of 18. (92.0) Neural folds elevated still further; fore-
the blastomeres; during gastrulaüon, the shape of the and hindbrain vesicles evident; two somites.
blastopore is used, and just after gastrulaüon the neural 19. (93.5) Neural folds approximate; mandibular
píate provides easily recognizable features. During or- arch marked by shallow groove; three so-
ganogénesis, the progress in the formation of the tail, mites.
limbs, gills, and mouth are convenient characteristics. De- 20. (95.0) Neural folds fused, except anteriorly;
velopment is, of course, conünuous, and the designated four somites.
stages gradually grade into one another. The amount of 21. (97.0) Neural folds closed to form neural tube;
time between successive stages vanes. For example, neu- four somites.
 LIFE HISTORY
128 22. (98.5) Head with opüc vesicles distinct; hy- prominent; gilí píate more distinct; 16 somites.
omandibular groove appears; five somites. 30. (133) Beginning of straightening of head cur-
23. (100) Head more prominent; mandibular arch vature and lengthening of trunk; 18 somites.
forming low ridge from neural cord ventrally 31. (140) Gilí folds become distinct ventrally; lens
to behind eye; six somites. pit and nasal pit visible; 19 somites.
24. (104) Hyobranchial groove appears; prone- 32. (150) Pericardial cavity present; straightening
phros pear-shaped; depression of otic cap- of head curvature about half complete; 20
sule visible; nine somites. somites.
25. (107) Head prominent; ear spot dorsal to hy- 33. (158) Muscular response; heart tube present;
omandibular groove; nine somites. 21-22 somites.
26. (110) Tail bud present; body begins to 34. (167) Heart tube more disünct; 24-25 so-
lengthen; gilí píate definite with shallow pit mites.
indicaüng formation of first branchial groove; 35. (169) Body curvature practically eliminated;
10 somites. heart beat; three externa! gilí nodules present;
27. (115) Stomodeum appears; 12 somites. balancer bud forms; chromatophores ap-
28. (119) Further elongaüon of body; greater pear.
prominence of head; first branchial groove 36. (180) Gilí buds definite; balancer bud prom-
distinct; 14 somites. inent.
29. (123) Tail bud well defined; head more 37. (192) Gilí circulation; forelimb bud.

Table 5-6. Jabíes of Normal Development of Amphibians

Cunrent dame Ñame used in pnblicatíon Reference
Caecilians
¡chthyophis glutinosus /chthyophis glutinosus P. Sarasin and F. Sarasin (1887-90)"

Salamanders
Hynobius nigrescens Hynobius nigrescens Usui and Hamsaki (1939)
Onychodacíy/us japonicus Onychodactylus japonicus Iwasawa and Kera (1980)
Andrias japonicus Megalobatrachus japonicus Rudo (1938)
Cynops pyrrhogaster Triturus pyrrhogaster P. L. Anderson (1943); Okada and Ichikawa (1946)
Echinotriton andersoni Tylototriton andersoni Y. Utsunomiya and T. Utsunomiya (1977)
Euproctus asper Euproctus asper Gasser (1964)
Notophthalmus uiridescens Triturus uiridescens M. Grant (I930b)b; Fankhauser (1967)
Pleurodeles walti Pleurodeles waltln Gallien and Durocher (1957)
Salamandra atra Salamandra atra Wunderer (1910)
Taricha torosa Triturus torosus Twitty and Bodenstein (1948)
Triturus alpestris Tritón alpestris Knight (1938); Fischberg (1948)
Triturus crisíatus Tritón cristatus Glücksohn (1931)
Trifurus heíueticus Triturus heíveticus Gallien and Bidaud (1959)
Triturus vulgaris Molge uulgaris Glaesner (1925)
Tritón taeniatus Glücksohn (1931)
Triturus taeniatus Rotmann (1940)
Tylototriton verrucosus Tylototriton verrucosus Ferrier (1974)
Necturus macu/osus Necturus macu/osus Eycleshymer and J. Wilson (1910)
Proteus anguineus Proteus anguineus Briegleb (1962b)
Ambystoma jeffersonianum Ambystoma jeffersonianum M. Grant (1930a)
Ambystoma maculatum Ambystoma punctatum R. Harrison (1969); Hará and Boterenbrood (1977)
Ambystoma mexicanum Ambystoma mexicanum Schreckenberg and Jacobson (1975); Bordzilovskaya and
Dettlaff (1979)
Ambystoma opacum Amblystoma opacum M. Grant (1930a)b
Eurycea bislineata Eurycea bislineata I. Wilder (1925)"
Plethodon cinereus Plethodon cinereus Dent (1942)

Anurans
Ascaphus truei Ascaphus truei H. Brown (1975a)
Xenopus laevis Xenopus laevis Weisz (1925); Nieuwkoop and Faber (1967); Deuchar (1975)
Alytes cistemasii Alytes cistemasii Crespo (1979)
Alytes obstetricans Alytes obstetricans Cambar and Martin (1959); Crespo (1979)
Bambino orienta/is Bambino orientalis J. Michael (1981)
Discog/ossus pictus Discog/ossus pictus Gallien and Houillon (1951)
Scaphiopus bombifrons Scaphiopus bombifrons Trowbridge (1941, 1942)
Caudiverbera caudiverbera Calytocephalella gayi Jorquera and Izquierdo (1964)

"Incomplete; temporal scale not ¡ncluded.

kPrimarily dealing with metamorphic stages.
 Eggs and Development
38. (210) Gills reach to base of forelimb bud; fila- 46. (525) Yolk completely absorbed; fourth fin- 129
mente developing on ventral ramus of each ger bud distinct; hatching.
gilí ramus.
39. (228) Gills reach to tip of forelimb bud; bal- The development of Ambystoma macu/afum at 20°C
ancer club-shaped. can be summarized, as follows: Stages 2-7 are times of
40. (252) Gills feathery, curved dorsally; forelimb cleavage and require about 17.5 hours. The blastocoel
bud slightly flattened distally; operculum dis- is formed in stages 8 and 9 (11.5 hours). Stages 10-12
tinct across venter; cornea transparent; pig- are gastrulation and require about 36 hours. Neurulation
mentation of iris visible. (stages 13-20) requires about 30 hours. Stages 21-29
€1. (315) Median notch of operculum evident; involve rapid growth of the head región including sensory
forelimb bud notched distally. capsules and require about 28 hours. In stages 30-35,
42. (330) Forelimb with deeper bifurcation dis- the body is straightened and the tail bud elongates; these
tally and slight bulge marking beginning of changes require about 46 hours. During stages 36-40,
elbow joint; gall bladder present. the gills and balancers develop, and the forelimb bud
43. (410) Mouth opens; hindlimb buds appear. takes on a paddle shape (83 hours). Stages 41-46 in-
44. (455) Forelimb longer, bowed slightly; first volve further development of the forelimbs, appearance
movements of forelimb. of hindlimb buds, development of the digestive system,
45. (500) Third digit of forelimb distinct; yolk stíll absorption of the yolk, and hatching; this is the longest
present in intestine. period of development, requiring about 273 hours.

Current na Ñame used in publication Reference

Hefeioporus eyrei Heleioporus eyrei Packer(1966)

EJeutherodactylus coqui Eleutherodactylus caqui Townsend and Stewart (1984)
EJeutherodactylus nubicola Eleutherodactylus nubicola Lynn (1942)
Physa/aemus biligonigerus Paludicola fuscomaculata Bles (1907)°
Pkurodema brachyops Pléurodema brachyops J. León and Donoso-Barros (1970)
Bufo andersonü Bufo andersonü Bhati (1969)
Bufo arenarum Bufo arenarum del Conté and Sirlín (1952)
Bufo bufo Bufo vulgaris W. Adler (1901)
Bufo bufo Cambar and Gipouloux (1957); Michniewska-Predygier and
Figón (1957); A. Rossi (1959)
Bufo maurantiacus Bufo maurantiacus Siboulet (1971)
Bufo melanostictus Bufo melanostictus Khan (1965)
Bufo regularís Bufo regularis Sedra and M. Michael (1961)
Bufo ualliceps Bufo ualliceps Limbaugh and Volpe (1957)
Nectophrynoides occidentalis Nectophrynoides occidentalis Lamotte and Xavier (1972)
Rhinoderma darwinü Rhinoderma darwini Jorquera et al. (1972)
Rhinoderma rufum Rhinoderma darwini Jorquera et al. (1974)
Gastrotheca riobambae Gastrotheca riobambae del Pino and Escobar (1981)
Hyla regi//a Hyla regula Eakin (1947)
Hyla auiuoca Hyla auiuoca Volpe et al. (1961)
Phyllomedusa hypocondria/is Phyllomedusa hypochondrialis Budgett (1899)"
Phyllomedusa trinitatus Phyllomedusa trinitatus Kenny (1968)"
Hemisus marmoratum Hemisus marmoratum Bles (1907)"
Rana arvalis Rana terrestris Michniewska-Predygier and Pigón (1957)
Rana breuiceps Rana breuiceps Mohanty-Hejmadi et al. (1979)°
Rana breuipoda Rana breuipoda Iwasawa and Monta (1980)
Rana chalconota Rana chalconota Hing (1959)°
Rana cyanophlyctis Rana cyanophlyctis Ramaswami and Lakshman (1959)
Rana dalmatina Rana dalmatina Cambar and Marrot (1954)
Rana esculenta Rana esculenta Michniewska-Predygier and Pigón (1957)
Rana japónica Rana japónica Tahara (1959, 1974)
Rana nigromaculata Rana nigromaculata Chu and Sze (1957)
Rana pipiens Rana pipiens Shumway (1940); A. Taylor and Shumway (1946)b
Rana syluatica Rana syluatica Pollister and J. Moore (1937)
Rana temporaria Rana fusca Moser (1950); Kopsch (1952)
Rana temporaria Michniewska-Predygier and Pigón (1957)
Rana tigerina Rana tigrina Khan (1969); Bhadi (1969); Agarwal and Niazi (1977)
Rhacophonis arboreus Rhacophorus arboreus Iwasawa and Kawasaki (1979)
Uperodon systoma Uperodon systoma Mohanty-Hejmadi et al. (1979)°
LIFE HISTORY
130

Figure 5-14. Early stages of normal development of a salamander, Ambystoma maculatum. Stages are
according to R. Harrison (1969). Guidelines indícate major features mentioned ¡n text.
 Eggs and Development
131

30

32
A

35 36
¡i 37

39

41

44 45 46

Hgnre 5-15. Later stages of normal development of a salamander, Ambystama maculatum. Stages are
according to R. Harrison (1969). Pigmentation is not shown. Guidelines indicate major features mentioned in text.
LIFE HISTORY
132 Xhe staging of salamander development generally is Anurans. The anuran stages (Figs. 5-17, 5-18) follow
not carried through to metamorphosis, as is characteristic Gosner (1960); hours given in parentheses after the stage
of the staging of anurans. However, 56 stages through number are for Bu/o valliceps at 25°C (Limbaugh and
metamorphosis have been defined in two European sal- Volpe, 1957).
amandrids: Pleurodeles walti (Gallien and Durocher, 1957)
and Triturus helvéticas (Gallien and Bidaud, 1959). 1. (0) Single cell; at fertilization egg rotates so
I. Wilder (1925) recognized four stages in the larva of that animal hemisphere is dorsal.
Eurycea bis/ineata: 2. (0.25) Second polar body released; gray
crescent evident.
1. Postembryonic: the brief period between 3. (0.50) First cleavage; 2 blastomeres.
hatching and feeding. 4. (1.00) Second cleavage; 4 blastomeres.
2. Typical larval: the typical feeding stage. 5. (1.50) Third cleavage; 8 blastomeres.
3. Premetamorphic: development of nasolabial 6. (2.00) Fourth cleavage; 16 blastomeres.
grooves but no vesicular glands in skin. 7. (3.00) Fifth cleavage; 32 blastomeres; cleav-
4. Metamorphic: morphological changes associ- age furrows irregular; dorsal cells (animal
ated with metamorphosis. hemisphere) smaller and completely cleaved;
ventral cells (vegetal hemisphere) larger and
Most developmental tables are for species having aquatic incompletely cleaved.
eggs and larvae. A developmental table is available for 8. (4.50) Midcleavage, characterized by contín-
only one species having direct development of terrestrial ued irregular cleavage and intrusión of pig-
eggs, Plethodon cinereus (Dent, 1942). Detailed descrip- mented área over palé área.
tions and illustrattons of postneurula development are 9. (6.50) Late cleavage; cells in animal hemi-
available for two other plethodontids having direct de- sphere are small, pigmented and extend well
velopment: Batrachoseps wrighti (Stebbins, 1949a) and down toward vegetal pole.
Ensatina eschscholtzi (Stebbins, 1954). 10. (8.00) Involution at dorsal lip of blastopore;
Rates of development are notably different between beginning of gastrulation.
species of Ambysíoma and salamandrids of the genera 11. (9.00) Dorsal lip of blastopore expands into
Cynops and Tarícha (Fig. 5-16). According to the staging semicircle; involuüon along semicircular sur-
tables for Pleurodeles walti (Gallien and Durocher, 1957) faces; balance of embryo shifts, raising blas-
and Triturus helveticus (Gallien and Bidaud, 1959), these topore.
salamandrids are like Cynops and Taricha Perhaps pat- 12. (10.5) Blastopore formed, surrounding yolk
terns of development reflect phylogenetic relaüonships, plug; blastopore elevated to point of poste-
but before any generalizatíons can be made, many other rior axis of embryo.
species, especially plethodontids, need to be studied in 13. (13.0) Dorsal flattening; formaüon of dorsal
detail and staged in a standard way. píate.

_, —' Stage 46 at 1008 hr

Figure 5-16. Comparative rates of A. Ambystoma maculatum. 20 C

development to the same stages (R. B. Ambystoma mexícanum. 18°C
Harrison, 1969) in four species of C. Taricha torosa, 17°C
salamanders. Data for Ambystoma D. Cynops pyrrhogaster, 18°C
maculatura from R. Harrison (1969),
for A. mexicanum and Tarícha from
Schreckenberg and Jacobson (1975), 60 120 240 360 480 600
and for Cynops from P. L. Anderson
(1943). Hours
 Eggs and Development
14. (16.5) Neural folds form as ridges lateral to 42. (499) Forelimbs protrude; angle of mouth 133
neural groove. (lateral view) anterior to nostril; labial den-
13. (19.0) Neural folds coalesce; body begins to ticles lost; horny beaks disappear.
elongate; embryo begins to rotate. 43. (546) Angle of mouth between nostril and
16. (22.0) Closure of neural folds, except ante- midpoint of eye; jaws and tongue formed;
riorly, to form neural tube; gilí plates distinct; tail begins to regress.
body elongated. 44. (596) Angle of mouth between midpoint and
17. (28.0) Tail bud; adhesive organs may begin posterior margin of eye; tail greatly reduced.
to develop. 45. (643) Angle of mouth at posterior margin of
18. (33.5) Muscular response; differentiation of eye; tail reduced to stub.
gilí arches; olfactory pits form. 46. (667) Tail resorbed; metamorphosis com-
19. (38.0) Heart beat; extemal gilí buds, if present plete.
at all, conspicuous.
20. (41.5) Gilí circulation begins. In summary, stages 1-7 are continuous cleavage, and
21. (51.5) Cornea transparent; mouth opens; ad- in stages 8 and 9 the blastocoel forms. Gastrulation oc-
hesive organs begin to disappear. curs during stages 10-12 and neurulation during stages
22. (58.5) Tail fins become transparent; circula- 13-16.Stages 17-21 involve the elongation of the body
tion begins in fins. and development of the tail bud, adhesive organs, and
23. (71.0) Opercular fold covers base of gills; lips gills. Stages 21-25 mark the transition from a relatively
and denudes begin to differentiate. immobile embryo sustained by yolk to a feeding and free-
24. (81.5) Opercular fold closes on right side. swimming tadpole. Mouthparts begin to develop in Stage
25. (91.0) Opercular fold closes on left; spiracle 23 and are essentially complete by Stage 25.The initial
forms. formation of parterns of pigmentation and the develop-
26. (115) Hindlimb bud appears; length of limb ment of the operculum generally occur in stages
bud less than half of its diameter. 23-25. Stages 26-40 involve growth of the larva and de-
27. (139) Hindlimb bud equal to or slightiy greater velopment of the hind limbs. Metamorphosis begins in
than half of its diameter. Stage 41 and is completed in Stage 46.
28. (163) Hindlimb bud equal to or slightiy greater The pattern of development of embryos developing
than its diameter. into aquatic larvae is generally the same in stages 1-16.
29. (188) Hindlimb bud equal to or slightiy greater Rates of development to different stages may be de-
than 1.5 times its diameter. pendent primarily on temperature and secondarily on
30. (235) Hindlimb bud equal to twice its diam- ovum size (Fig. 5-19). Hatching may occur at any time
eter. after Stage 16.
31. (259) Foot paddle-shaped; no interdigital in-
dentations. Caecilians. The development of the caecilian ¡chthy-
32. (283) Margin of foot indented between fourth ophis glutinosus has been described and beautifully il-
and fifth toes. lustrated by P. Sarasin and F. Sarasin (1887-90), but
33. (306) Margin of foot indented between third comparison with salamanders and anurans is difficult be-
and fourth, and fourth and fifth toes. cause no times were given for the duration of the various
34. (332) Margin of foot indented between sec- stages. However, some similarities and differences are
ond and third, third and fourth, and fourth apparent. During neurulation, the embryo elongates tre-
and fifth toes. mendously, so as to be curved over the top of the large
35. (356) Margin of foot slightiy indented be- yolk sac. The anterior ends of the neural folds cióse, and
tween first and second toes. regions of the brain begin to differenüate before the neural
36. (379) First and second toes joined; others tube is closed posteriorly (Fig. 5-20A). Nasal, optic, and
separated. otic capsules form at about the same time as the man-
37. (403) All five toes separated. dibular and hyoid arches and the gilí buds (Fig. 5-20B).
38. (415) Inner metatarsal tubercle formed. By the time the mouth is open, the eyes, gills, and lateral-
39. (427) Pigment-free patches on ventral sur- line system are well developed (Fig. 5-20C).
faces of toes .where subarticular tubercles will
develop.
40. (451) Subarticular tubercles formed; cloacal HATCHING AND BIRTH
tail-piece present. Embryonic amphibians enter the external environment
41. (475) Skin over forelimbs thin and transpar- by escaping from the egg capsules either as larvae or as
ent; larval mouthparts begin to break down; miniature replicas of the adults, or by leaving the body
cloacal tail-piece lost. of the parent.
LIFE HISTORY
134

Fertilizaron Gray Crescent 2-Cell 4-Cell 8-Cell

16-Cell 32-Cell Mid-Cleavage Late Cleavage Dorsal Lip

Mid-Gastrula Late Gastrula Neural Píate Neural Folds Rotation

16 17 18 19

Neural Tu be Tail Bud Muscular Response Heart Beat

21 22

Gilí Circulation Cornea Transparent Tail Fin Circulation

Operculum Development
Figure 5-17. Standard early stages of development of anurans. Stages are according to Gosner (1960).
Guidelines indícate major features mentioned in text.

Hatching lip (Fig. 5-21) is effective in cutting the tough egg capsules
Two basic mechanisms are associated with hatching. One while sharp movements are made by the head. Once the
of these, the egg tooth, is mechanical; so far it is known egg capsules have been cut, the froglet pushes its head
only in frogs of the genus Eleutherodactylus. This small, through the incisión, then pulís its forelimbs free, and
usually bifid, structure on the median margin of the upper climbs out of the egg.
 Eggs and Development
135
26 27 28 29 30

snn» L<1/2xD LslxD

Limb Bud (Length:Diameter)
L=2 xD

31 32 33 34 35

\X

36 37 38

m~~*~&..

J^
Toe Development Subarticular Tubercles
40 42

Cloacal Tail Piece Forelimb Emerged

Forelimb Larval Mouthparts Gone

Mouth Development and Tail Resorption

Figure 5-18. Standard later stages of development of anurans. Stages are according to Gosner (1960).
Pigmentation is not shown. Guidelines indícate major features mentioned in text.

The second, and more widespread, hatching mecha- A dual hatching process occurs in salamanders, except
nism is chemical. Frontal glands are scattered over the plethodontids. Hatching from the vitelline membrane oc-
snout and nape or concentrated on the snout of embryos. curs just after neurulation; thus, the embryo comes to lie
These glands produce hatching enzymes, which are pro- in the capsular fluid formed by previous dissolution of
teinaceous proteases capable of digesting gelatin and other the inner mucoid capsule (Salthe, 1963). Hatching from
proteins but not active against mucopolysaccharides (Mi- the egg capsules occurs much later, at a stage when at
ganü and Azzolina, 1955). Antiproteolytic factors identi- least the forelimb buds are present. The vitelline mem-
fied in embryos by Wu and Wang (1948) presumably brane remains intact until hatching in plethodontids.
protect the embryos from their own hatching enzymes. Anurans in which later development occurs in a cap-
Possibly there is more than one kind of hatching enzyme sular chamber (Alytes, Díscoglossus, Pipa, and probably
produced at different times by a given species, for dif- Eleutherodactylus) hatch first from the vitelline mem-
ferent electrophoretic components were identified in brane and much later from the capsules (Salthe, 1963).
hatching enzymes at different stages of development in Possibly the first hatching is accomplished by hatching
Rana pipiens (Salthe, 1965). enzymes in Eleutherodactylus, while only the escape from
LIFE HISTORY
136
25-

B C
20-

15-

10-
Figure 5-19. Comparative rates of A. Bufo valliceps, 25°C
development to hatching ¡n five B. Xenopus laevis, 18°C
species of anurans. Developmental C. Rana sylvatica, 18.4°C
stages follow Gosner (1960). Data for 5- D Phyllomedusa tarsius
Bufo oalliceps frota Limbaugh and E. Rana pipiens, 18°C
Volpe (1957), for Xenopus laevis from
Weisz (1945), for Rana sylvatlca
from Pollister and Moore (1937), for
Phyllomedusa trinitatus from Kenny O 30 60 120 180 240 300
(1968), and for Rana plpiens from
Shumway (1940). Hours

Otic
vesicle Hindbrain
Midbrain IV
Optic
vesicle
II (Hyoid)
Olfactory
vesicle (Mandibular)
Forebrain
Figure 5-20. Stages in the
development of the caecilian
Ichthyophis glutinosas:
A. Neurulation. B. Early
organogénesis. C. Late development.
Branchial arches are designated by
román numeráis. Redrawn from F.
Sarasin and P. Sarasin (1887-90).

the egg capsules is accomplished by the egg tooth, a

structure not present at the time of hatching from the
vitelline membrane.
Two other patterns of hatching are known in anurans.
In some bufonids, leptodactylids, and hylids, the outer-
most capsules split open and the inner capsules emerge
from them prior to the hatching of the embryo. This type
of hatching occurs in various kinds of aquatic eggs, such
as those of Xenopus laevis (Bles, 1905), and may result
from differential swelling of capsules. At least in Bufo
bufo, this type of hatching occurs before the frontal glands
develop (Kobayashi, 1954). In other anurans, hatching Figure 5-21. Egg tooth on margin of upper lip in
occurs first through the vitelline membrane and then ElKutherodactytus rugulosus. Rapid movements of the head result
through the capsules; the entire process is continuous in the egg tooth cutting through the egg capsules.
and rapid.
Final escape from the capsules is accomplished by glid-
ing through the degenerating membranes in at least some al., 1961). In other frogs, the weakened membranes are
Bufo and Hyla, in which the outer capsules rupture first; ruptured by violent muscular actions of the embryos.
ciliary acüon has been suggested as the mechanism for Hatching of the arboreal eggs of Phyllomedusa trinitatus
this relatively passive escape (Kobayashi, 1954; Volpe et is rather explosive (Kenny, 1968); presumably such a
 Eggs and Development
i hydrostatic pressure develops in the eggs that when pairs of gilí stalks; those parts of the gills that are adjacent 137
: te wtelline membrane is weakened by hatching enzymes to the female are adherent to the thin egg capsule, which
i fe membrane bursts, hurling the tadpole free of the leaves. remains fastened to the female. Subsequently, the stalks
The mode of hatching is known for relatívely few spe- are broken; the froglets depart, and the gills and stalks
¡ «fes of amphibians. The ways in which amphibian eggs are sloughed from the female. In those egg-brooding hy-
í mtch seem to be more closely associated with their mode lids in which the eggs are brooded in a dorsal pouch on
1 m¿ site of development than with their phylogeneüc re- the female, the eggs hatch into tadpoles or froglets in the
I fcfcnships. The trigger for activation of hatching enzymes pouch. Parturiüon from the pouch may be simply by
;' •mst. be reduced oxygen pressure, as noted in aquaüc pressure exerted by the female flexing her shoulders and
I «£s of some salamanders and anurans (Petranka et al., breathing deeply (Duellman and Maness, 1980). As the
I BE). young emerge, the large external gills are broken off and
lost (Fig. 5-23). In those species of Gastrotheca having
small pouch apertures, the female aids in the parturiüon
Enbryonic development and metamorphosis are com- of tadpoles or froglets by insertíng her hindfeet into the
i pfeted in the uterine porüons of the oviducts in Sala- pouch and digging out the young.
1 manara otra and Mertensietta luschani, one species of Males of Assa dar/ingíoni carry tadpoles in paired in-
Beutherodactylus (¡aspen), several species oíNectophry- guinal pouches, where they develop into froglets
motdes, and many species of caecilians. In these animáis, (Straughan and Main, 1966). There is no evidence that
Ifae young emerge from the cloaca as miniature replicas the male aids in the escape of the young. The tadpoles
cí the adults, although in caecilians the newborn young of Rhinoderma darwinii develop into froglets in the vocal
Hay be 40% of the length of the mother. sac of the male. These froglets crawl from the vocal sac
The young of several kinds of frogs are carried by their into the mouth and then to the exterior. Obviously the
párente and develop in specialized brooding pouches. escape of the young requires the cooperation of the male,
The aquaüc frogs of the genus Pipa carry eggs imbedded who presumably opens his mouth in response to the
in the dorsum of the female. Upon completion of devel- movement of the froglets.
opment, the froglets push their way out of the aperture Certainly the most bizarre example of egg brooding
of the dermal chamber and swim away (Fig. 5-22). Sim- and birth in amphibians is that of Rheobatrachus si/us
iariy, tadpoles emerge from the chambers in Pipa car- and R. vitetiinus. Tadpoles develop in the female's stom-
aalhoi. ach. Birth is accomplished by the female opening her
Among the egg-brooding hylid frogs, hatching of the mouth and greatly dilating the esophagus. The young are
eggs carried on the dorsum by female Hemiphractus re- almost propelled out of the stomach into the mouth, and
suhs in froglets attached to the dorsum of the female by they hop away (Tyler and Cárter, 1981) (Fig. 5-24).

Figure 5-22. Young of Pipa pipa

emerging from dorsum of female.
Photo by J. Lescure.
LIFE HISTORY
138

Fignre 5-23. Young emerging from

the pouch of a female Gastrotheca
ovifera. The externa! gills
surrounding the embryo are either
broken off during parturition or
sloughed soon after birth. Photo by
S. J. Maness.

Figure 5-24. Oral birth of

Rheobatrachus silus. Young develop
in the stomach and are expelled from
the mouth. Photo courtesy of M. J. MÍi|JÍÍBÍ HK,
Tyler.
 Eggs and Development
DEVELOPMENT AND have well-developed internal gills. However, anuran em- 139
AMPHIBIAN DIVERSITY bryos developing on land have either large external gills
The three living orders of amphibians have the same or other respiratory tissues—expanded tails or lateral folds.
baac egg structure and development, but different kinds The diversity of embryonic respiratory structures is a re-
of adaptations and specializations are evident in each flectíon of the different environmental conditions in which
aroup. Some of these adaptations and specializations seem embryos develop, as well as precursors to larval respi-
to be correlated with highly specialized reproductíve modes, ratory mechanisms—external gills in salamander larvae
whereas others seem to be associated with, and perhaps and internal gills in anuran larvae.
íesponsible for, broad ecological tolerances and wide Information on basic metabolic rates of amphibian em-
geographic distributions. bryos is very fragmentan/. Salamander eggs seem to re-
The common occurrence of polyspermy in salaman- quire more nutrients and more time to develop than do
ders having a spermatheca is understandable when it is those of anurans. At the present time there is no reason-
realized that the eggs pass by a concentration of captive able explanatíon for these differences. However, the rel-
spermatozoa. This method of insemination insures a high atívely rapid rate in anuran embryos is partially reflected
percentage of ferülization and necessitates immediate in their ability to tolérate higher temperatures than sala-
swelling of the egg capsules to block the entrance of mander eggs. The wide range of developmental toler-
addiüonal sperm. Monospermy is the rule in anuran eggs, ance levéis in anuran embryos also is associated with a
in which the eggs are placed in water and capsular swell- diversity of clutch structure, which is important in heat
ing begins immediately prior to insemination. Penetration retention and dissipation.
of the ovum by a single spermatozoon results in the Some members of all three orders of living amphibians
breakdown of cortical granules into the perivitelline fluid are viviparous. The methods of obtaining maternal nu-
and prevention of the entrance of additional spermato- trients are different in the three groups and are especially
zoa. It is doubtful if any anuran eggs are ever subjected well developed in caecilians, in which viviparity is com-
to the concentration of spermatozoa that await the pas- mon. In this respect caecilians may be regarded as the
sage of eggs by the spermatheca in salamanders, al- most highly derived group developmentally, but their highly
though this might be true in those ovoviviparous and specialized morphology and mode of existence have lim-
viviparous anurans having internal fertílization. ited their evolutionary and geographic diversity.
The absence of cortical granules in salamander eggs Salamanders seem to have the simplest patterns of
may be related to the early liquefication of the innermost development and the fewest modifications of the gen-
capsule in these eggs, as opposed to retention of a highly eralized amphibian development. This conservativeness
viscous inner chamber in most anurans. Likewise, the is reflected in the relatívely narrow ecological and geo-
sequence of degeneraüon of capsules seems to be related graphic diversity of the group, as compared with anurans.
to the method of hatching. However, these attributes of Probably, the great diversity of anurans, both ecologically
amphibian eggs are known for few species, most of which and geographically, is associated with their develop-
have aquatic eggs. mental plasticity, as evidenced by their diversity of egg
Embryonic respiratory structures and mechanisms are and clutch structure, temperature tolerances, respiratory
relatively simple in salamanders. The degree of devel- mechanisms, metabolic excretory products, and hatching
opment of the external gills in species having aquatic processes.
larvae seems to be associated with the environmental Given the recent emphasis on the importance of on-
conditíons in which the larvae will develop, but for the togeny to the understanding of adaptations and phylog-
most part, the same conditíons prevail for the developing eny (e.g., S. Gould, 1977), much more must be learned
eggs—different oxygen tensions in stagnant versus flow- about patterns of development and embryonic metabo-
ing water. The significance of the different structural types lism in order to support or falsify many of the hypotheses
of external gills in embryos of terrestrial plethodontíd sal- being advanced. Descriptíve embryology has been out
amanders is unknown. Developing caecilians have ex- of vogue for many years, during which time develop-
ternal gills, but these functíon solely within the egg or mental biologists have emphasized molecular and bio-
maternal oviduct, for the gills are resorbed immediately chemical aspects of development. However, the answers
after hatching in those that have free-swimming larvae to many fascinating problems of amphibian development
or immediately before birth in oviparous and viviparous are dependen! on many more comparativa embryologi-
caecilians. External gills are absent or transient in em- cal studies in an evolutionary context of the development
bryos of most anurans; those that have aquatic tadpoles of the embryo in its natural environment.
 CHAPTER 6
fti patterns o/adaptíve radiation, the larvae
WÍiÍÍÍÍÍ& m
ofa taxonomía unit share certain major
eftaracfers, but in other respecte they show Wiiiiiiiift^
•
évergent modifications that adapt them to
difjeretti ecológica! conditions or different
•Kl:í$&$.i#:$:;::<^
':<!m^\-.*ZM*!íy*y':.?Kí®$:8y!&¿3 I
•ais oflife.
Grace L. Orton (1953)

A Lmphibian larvae represen! posthatching develop-

mental stages that are morphologically disünct from the
The habitus of amphibian larvae are as diverse as their
ufe styles. Typically, anuran tadpoles are found in streams
adults and are nonreproducüve. Most larvae obtain nu- and ponds or ephemeral situations such as puddles and
trients from the environment for further development and roadside ditches, where they glean food by scraping it off
growth. The majority are aquatic and thus are subjected the substrate or feeding on parücles suspended in the
to different selective pressures than the adults. Larvae of water. Their specialized feeding habits require mouth-
salamanders and caecilians more closely resemble their parts and a digestive system that is dramaücally different
respective adults morphologically, physiologically, and from those characteriáng the adult frog. The adult is short-
trophically than do anuran larvae. bodied and tailless, but the larva possesses a tail and
This chapter treats the morphology, physiology, ecol- usually well-developed caudal fins in order to propel itself
ogy, feeding, growth, and social behavior of amphibian through the water. Salamander and free-living caecilian
larvae. Most of the material on larval morphology is cov- larvae also are found in aquatic situations, but unlike
ered here, but early embryonic development is covered short-bodied tadpoles, these larvae are elongate. The
in Chapter 5 and most aspects of metamorphosis are presence of a fin along the tail, and on the back of some
treated in Chapter 7. Populatíon dynamics and com- as well, enables them to swim effectively; moreover, the
munity ecology of larvae are discussed in chapters 11 larvae, like the adults, are active predators. Conse-
and 12, respectively. quently, larval salamanders and caecilians have func-
tional jaws, teeth, and an adult-like digestive system at
the time of hatching, or shortly thereafter.
MORPHOLOGY OF LARVAE The similarity of salamander and caecilian larvae to
Operationally, a vertébrate usually is described by its ex- their respective adult morphs may account for their pro-
ternal characteristics—that is, its general size and shape, tracted embryonic development prior to hatching in con-
presence or absence of obvious features, and relaüve trast to that of most anuran larvae. Although the timing
proportíons of parts of the body. Most of these charac- of hatching varíes considerably among anurans, it can
teristics reflect differences in the structure of the musculo- occur as early as the tail-bud stage (early post-neurula-
skeletal system that supports and protects vital organs üon; e.g., Bufo). In salamanders, hatching occurs sub-
and provides for locomotory and feeding movements. sequent to development of the mouth and internal or-
141
LIFE HISTORY
142 gans; gills are present and the digits on the forelimb are is flanked laterally by mesoderm that gives rise to somites.
differentiatíng, but the hindlimb is present only as a bud. Concomitant with the formation of the neural tube, a
When caecilians hatch, they are distinguished externally group of uniquely important cells—the neural crest cells—
from adults only by the presence of a tail fin posteriorly migrate from the external surface of the epidermis to its
on the body, an open gilí slit, and external gills in some. internal surface. Here they lie between the epidermis and
The disparities in the timing of hatching, both within
and among the orders of amphibians, make it especially neural píate
difficult to describe larval morphology that changes con-
tinuously. Nonetheless, there are certain commonalities
of developmental form and function among all three groups
that are worthy of comment. For example, all amphibian
larvae are elongate and usually not well ossified. The
brain and priman/ sensory organs are protected by car-
-neural fold
tilage—the chondrocranium that is composed of olfactory (neural crest cells)
and auditory capsules and the cartilaginous precursors of
the sphenethmoid, prootíc, and exoccipital that protect
the brain. The mandibular arch is developed and variably
ossified depending on larval feeding habits, but it is al-
ways present. All amphibian larvae possess a cartílagi- -ectodermal
nous hyoid arch and branchial arches, although the latter epithelium
may be modified for special feeding and respiratory func-
tions. Lateral-line sensory organs are present. The skin
is thin and the eyes lack any protective covering. There
are some striking differences as well as similarities among
the orders of amphibians in the development and adult
morphology of the skin, and in the urogenital and diges-
üve systems. Because these are described elsewhere in neural crest
association with metamophosis, emphasis is placed here cells epidermis
on ectodermal and mesodermal derivatives that give rise
to the musculoskeletal system and, therefore, determine
the overall, external appearance and body plan of the
larva. Although a discussion of organogénesis is in the
province of developmental biology (and early organo-
génesis is described in Chapter 5), the following descrip-
neural crest
tion provides informaüon relevant to an understanding cells
and appreciation of the development of the larval
musculoskeletal system in particular.

Basic Pattern of Development

neural tube
Despite the readily recognized differences among fully
formed, premetamorphic amphibian larvae, the course
of primary organogénesis of ectodermal and mesodermal Figure 6-1. Stages in the formation of the neural píate and neural
components is remarkably similar in its pattern. At the tube in anurans. On the left are diagrammatic representations of
completton of neurulation (the earliest stage at which any embryos and the plañe of section (heavy line) corresponding to the
schematic transverse sections on the right (neural crest cells are
amphibian is known to hatch and therefore be classified black). Embryos designated A-E approximate Gosner's (1960)
as a larva), the neural tube overlies the notochord and stages of development 12F-13, 14, 15, and 17, respectively.

(—mandibular r-ear vesicle ,-ear vesicle

-hyoid ^branchial arch 1 -branchial arch 1
branchial arches i—branchial arches 2-4 ,-branchial arches
2-4

Figure 6-2. Three successive stages

(left to right) in the migration of
neural crest cells in the salamander
Ambystoma maculatum. Redrawn
from B. Balinsky (1960). -eye mandibular—1 L-nvciid mandibular-1 "-maxillary
 Larvae
te mesoderm (Fig. 6-1). As they migrate throughout the rarea of fusión 143
áeveloping embryo or larva, neural crest cells give rise trabecula- f—parachordal
lo a variety of important structures. Some produce pig-
•ent cells and thereby establish the basic color and pat-
fcm of the larva. Others that come to lie in the head
«gon produce the visceral skeleton (i.e., quadrate,
Meckel's cartilage, hyoid, and first branchial arch), the
papillae of the teeth, and the rudiments of the anterior
haif of the chondrocranium. The action of neural crest
cefls in association with the formation of primary brain
•eskles and the rudiments of the eyes from the anterior
pan of the neural tube establishes the generalized, early
«nphibian embryonic or larval form in which the body
B subdivided into a head and trunk separated by visceral
defts and arches posteroventral to the head (Fig. 6-2).
Subsequent development involves interactíons of ec- olfactory
todermal and mesodermal components that produce the capsule
eye capsule-1
brval chondrocranium, visceral skeleton, axial and ap-
notochord—1
pendicular skeletons, mouth, fin, external gills and bal-
ear capsule-1
ancers, and somatic musculature. Owing to the com- 1st vertebra— 1
piexity of these events and structures, they are described
separately. Figure 6-3. Schematic representation of the components of an
amphibian chondrocranium in dorsal view. Initial stages of
cartilaginous components are stippled. Áreas in which cartilaginous
Chondrocranium. The chondrocranium and anterior elements eventually will fuse are indicated by hatching in upper or
elements of the first visceral arch (palatoquadrate and right-hand side of diagram. Redrawn from B. Balinsky (1960).
Meckel's cartilage) house and protect the brain and pri-
mary sensory organs, and provide a mechanism for larval ascending process 1st vertebra
feeding. Earliest development (Figs. 6-3, 6-4) is marked orbital cartilage-| rear capsule
by the appearance of a procartilage bar (the palatoquad- oculomotor
rate) anterior to the second visceral pouch (which be- foramen fenestra ovalis
comes the tympanic cavity). The dorsal, vertical com- pila metoptica
ponent of this bar is the quadrate, the element that optic foramen-j
suspends the mandibular arch from the neurocranium. A
preoptic i
horizontal component, Meckel's cartilage, extends for- root
ward from the base of the palatoquadrate and, in the
adult, forms the lower jaw in combination with dermal
investing bones. Subsequent to the appearance of the
palatoquadrate, longitudinal bars of procartilage arise
medial to it. The bars (cranial trabeculae) increase in length
and mass. Anteriorly, the bars fuse medially; their various
outgrowths eventually give rise to the cartilaginous com-
ponents of the nasal capsule. Posterior to the nasal cap- -trabecula
sule, the sphenethmoid will form in the trabecular carti-
Meckel's cartilage-
lage; in the adult, this bone forms the posterior walls of (mandible)
the nasal capsule and the anterior braincase. The cranial quadrate—1
trabeculae extend posteriorly and attach to the sides of hyoid arch-1
the anterior tip of the notochord. As the posterior tra- parachordal—1
beculae increase in mass, they become integrated with basibranchial 2-1
the developing auditory capsules and connected to the branchial arches 1-4-1
palatoquadrate laterally by means of a lateral outgrowth.
In this way, the cartilaginous precursors of the prootic Figure 6-4. Lateral view of the chondrocranium and visceral
skeleton of a salamander larva. Structures labeled ascending
and exoccipital, which form the posterior end of the process and quadrate compose the palatoquadrate; see text for
braincase in the adult, are established. Integration of the further explanation. Redrawn (in part) from B. Balinsky (1969).
cartilaginous auditory capsules laterally completes the ru-
diments of the posterior región of the skull, and the es- Visceral Skeleton. The branchial región of all am-
tablishment of a connecüon with the palatoquadrate as- phibian larvae is pierced by a series of five or six clefts,
sures the continuity of the suspensorium—the mechanism or visceral pouches. The first and most anterior of the
by which the jaws are connected to the braincase. series lies between the developing Meckel's cartilage and
LIFE HISTORY
144 hyoid and is incorporated into the tympanic cavity. This layer of the skin. A somatic cavity (the myocoele) inter-
pouch never opens to the outside in salamanders and nally sepárales this outer layer from the internally that
frogs; in caecilians, however, it is open briefly, during produces the somatic musculature. The ventromedial
which time it acts as a spiracle. Posteriorly, four (sala- portion of each somite is composed of the sclerotome.
manders and frogs) or five (caecilians) more pouches This portion breaks up into mesenchyme cells that mi-
form. The pharyngeal wall between these clefts is sup- grate and continuously envelop the notochord and spinal
ported by bars of cartilage that represent the hyobran- cord. Subsequently, the mesenchyme cells differentiate
chial apparatus (Fig. 6-4). The most anterior and gen- into cartilaginous nodules, the arcualia, to form the cen-
erally the most substantial of these elements is the tra, transverse processes or ribs, and the neural arches
ceratohyal (hypohyal) that lies between Pouches I and II of the developing vertebrae.
(see Fig. 6-7). The lateral components either articúlate
with, or are fused to, a midventral, longitudinal element Appendicular Skeleton. Among those amphibians
or series of elements known as copulae or basibranchials. that have limbs (i.e., salamanders and anurans), the limb
The ceratohyals and their associated midventral basi- buds are the first trace of the appendicular skeleton. Aside
branchials form the hyoid píate and its anterior processes from nerves and blood vessels, the primary components
which, in the adult, represent the skeletal platform from of limb buds are lateral píate mesoderm, epidermis, and
which various tongue muscles origínate. Posterior to the somites. Initial limb-bud formation involves migration of
ceratohyals is a series of four pairs of ceratobranchials mesenchyme cells from the upper edge of the parietal
(I-IV), carülaginous bars that sepárate Pouches II, III, IV, surface of the lateral píate mesoderm to the inner surface
and V. These either are fused midventrally or articúlate of the overlying epithelium in two áreas—one just pos-
with basibranchials to form the posterior part of the hy- terior to the branchial región and a second just anterior
olaryngeal apparatus. to the anus. As the mesenchyme proliferates internally
and the overlying epidermis thickens, the limb bud pro-
Axial Skeleton. The vertebral column is mesodermal trudes. Once the limb bud has grown to the point that it
in origin and formed from the association of the somites is longer than broad, subordínate parts of the limb begin
that flank the neural tube and notochord (Fig. 6-5). The to differentiate in a proximodistal sequence. Thus, the
cells composing each somite are differentiated into three upper arm and leg (stylopodium) are established before
types. The most dorsal type is the dermatome that is the lower segments (zeugopodium), and the latter prior
continuous with, and gives rise to, the connective üssue to the distal elements (autopodium). Among the distal
elements, however, the proximodistal scheme of devel-
opment does not prevail; larger skeletal elements (i.e.,
-spinal cord
l—myotome
metatarsals and metacarpals) differentiate prior to smaller
i—limb rudiment limb bud—i ones (i.e., carpáis, tarsals, and phalanges). Proximal
phalangeal elements form before distal ones. Thus, digits
I and II develop before III, IV, and V (when present),
and the latter form in the sequence of their numbers.
Because fusión of individual cells into masses (myoblasts)
provides the rudiments from which the limb muscles
eventually develop, limb muscles presumably are formed
by the migration of these cells from the myotomes into
renal the developing limb.
tubule
Of the mesenchyme cells that migrate from the parietal
surface of the lateral- píate mesoderm, the central cells
are destined to form the limb bud proper, whereas the
peripheral cells give rise to the pectoral and pelvic girdles.
Thus, development of girdles is associated closely with
that of limbs, but it is independen! because girdle for-
parietal mation proceeds independently of the direct mesenchy-
layer of mal-epidermal interaction that is essential to limb devel-
lateral
píate
opment. However, normal formation of articular facets
of the girdles is dependent on the formation and presence
endoderm of upper limb elements.
visceral layer of
lateral píate Characteristic Epidemial Structures. During neu-
rulation the epidermis is separated from other ectodermal
Figure 6-5. Diagram of the origin of limb bud mesoderm in an components (i.e., neural píate and neural crest). In ad-
amphibian embryo. Redrawn from B. Balinsky (1960). dition to the skin, several other important structures are
 Larvae
derived from the epidermis. Among these are the lens of Orbital cartílage = orbital cartílage + taenia marginalis 145
the eye, the cornea, cranial ganglia, the ear, and nasal of caecilians
organ. By a series of complicated inducttons involving Palatoquadrate = quadrate + ascending process +
the developing brain and sensory organs, protective car- otic process + pterygoid process
daginous capsules are laid down and eventually incor- Planum termínale = lamina orbitonasalis of caecilians
porated into the developing chondrocranium. Posterior basicapsular commissure = occipital arch of
Other epidemial structures are simple protrusions. These caecilians
rnclude the fin, extemal gills, balancers and barbéis, and Pterygoid process = basal process
the paired limbs described above. A depression in the
superficial ectodermal epithelium, the stomodeum, marks Caecilians
Ae invaginatíon of the mouth. When the internal, en- The striking feature that characterizes caecilian larvae in
dodermal epithelium of the alimentary canal fuses with contrast to salamander and frog larvae is the advanced
tfie external epithelium, the pharyngeal membrane is stage at which they hatch. Superficially, larvae are distin-
formed. The mouth opens when this membrane disap- guished from adults only by their smaller size, the pres-
pears. A similar membrane is formed between the ecto- ence of a gilí slit, and a fin in those larvae that meta-
derm and endoderm at the base of the tail bud. As the morphose into terrestrial adults (ichthyophiids,
tail lengthens, the cloacal membrane produces a diver- rhinatrematíds, and some caeciliids). Any discussion of
ficulum (post-anal gut) that enters the tail rudiment. caecilian larval morphology is hampered by a lack of
Depression of the superficial epithelium in this área pro- knowledge; the only caecilians having aquatíc larvae for
duces the proctodeum; once the cloacal membrane rup- which there are developmental observations are ¡chthy-
tures, the cloaca is open to the exterior. ophis g/utinosis (P. Sarasin and F. Sarasin, 1887-1890;
Peter, 1898), Typh/onectes obesus (M. Wake, 1977), and
Nomenclatura of Chondrocranial and Visceral Gegeneophis carnosus (Ramaswami, 1948). The work
Elemente. The descriptíve accounts of chondrocranial of Brauer (1897, 1899), H. Marcus (1909, 1910, 1922),
and visceral components of caecilians, salamanders, and Gewolf (1923), H. Marcus et al. (1933, 1935), and Law-
anurans that follow are generalized. Sufficient informa- son (1963) described Hypogeophis rostratus and Gran-
1k>n is provided so that the reader can grasp the basic disona altemans; M. Wake (1980a, 1980b) and M. Wake
architectural plan of each group in order to appreciate and Hanken (1982) have contributed substantially to un-
their gross similarities and differences, but details of var- derstanding the development of Dermophis mexicanus.
iation are beyond the scope of this book. The descrip- But Dermophis is viviparous and Hypogeophis and
tions present the basic architecture and terminology ap- Grandisonia are oviparous with direct development. It
plied to amphibian chondrocrania, so that a better remains to be demonstrated that the developmental ob-
understanding may be gained from technical papers and servations on these species are applicable to those taxa
monographs, such as de Beer (1937), that deal exhaus- having aquatic larvae, although M. Wake (1977a) sug-
tively with the structure and development of the skull. gested that they are.
Except for the oíd and rare review paper of Gaupp
(1906), no one person has dealt with the cranial devel- External Features. Free-living larval caecilians are
opment of all three orders of amphibians. Thus, termi- proporüonally shorter than adults. They are characterized
nology of elements frequently is not the same across the by thin skin, long triramous gills, a lateral-line system,
three orders, and at this point, knowledge is so incom- adult dentition, and a modérate tail fin that extends onto
plete that it is not possible to solve the existing problems the posterodorsal surface of the body. The eyes of "ma-
of homology. In many cases, terms have been used in- ture" larvae are covered by skin and bone. The tentacle,
terchangeably in the literature. In order to simplify the which does not appear untíl metamorphosis, is absent.
following descriptions, the following nomenclatural con-
venüons have been adopted: Chondrocranium and Mandible. In comparison with
the chondrocrania of salamanders and anurans, that of
Alary cartílage = cupular carülage of caecilians caecilians is highly fenestrated and delicate (Fig. 6-6).
Anterior trabecular píate = internasal píate, ethmoid The floor of the chondrocranium lacks a basal píate be-
píate, planum intemasalis, planum trabecula anterior tween the auditory capsules; the capsules are united pos-
Basal píate = planum basalis teriorly by a bar—the hypochordal commissure that in-
Basibranchials I-II = Copulae I-II corporales the anterior típ of the notochord medially and
Basitrabecular process = basipterygoid process, ? otic the poorly developed auditory capsules laterally by means
process of some authors of a lateral outgrowth, the posterior basicapsular com-
Ceratobranchial = branchial missure. Paired, anterior extensions (cranial trabeculae)
Ceratohyal = hyale that unite anteromedially behind the olfactory capsule
Cranial trabecula = cornua trabecula endose an immense ventral fenestra that represents a
Hypochordal commissure = planum hypochordialis unión of the anterior and posterior basicranial fenestrae.
LIFE HISTORY
146 palatoquadrate-
orbital c.- retroarticular proc. (Meckel's c.¡
pila antoptica-
preoptic root-
Meckel's c. auditory capsule
solum nasi jugular f.
alary c. cranial trabecula
prenasal proc.
(basicranial fen hypochordal
commissure
mfranarial c. prootic f.
oblique c
septum nasi
planum terminale-
mternasal píate- 1 L O rbitonasal f.

ppalatoquadrate
oculomotor f orbital c. ascending proc. basal proc.
Meckel's otic proc.
auditory capsule t
planum antorbitale
cavum internasale

solum nasi
L occipital
condyle .
tectum planum precerebralejt
¡nternasale optic f.- tectum synoticum ™
prootic f.- frontoparietal fen. jugular f-

D palatoquadrate taenia tecti - otic proc.-

medialis ascendmg proc.- fen. ovalis
cornu trabecula
suprarostral c. perilymphatic ff.

tectum
synoticum

infrarostral c.-1 jugular f.

suprarostral c. taenia tecti píate
proc. marginalis -basicranial fen.
muscularis quadrati frontoparietal fen. L cranial trabecula
-trabecular píate
Figure 6-6. Chondrocrania of amphibian larvae. A. Dorsal view of Ichthyophís glutinosas. B. Dorsal view
of Salamandra salamandra (total length 20 mm). C. Ventral view of same (without mandible). D. Dorsal
view of Rana temporaria (total length 29 mm). E. Ventral view of same. Abbreviations: c = cartilage;
f = foramen; fen = fenestra; ff = foramina. Redrawn from Gaupp (1906).

Dorsal extensions from each trabecula, the pila antoptica drocranium. The chondrocranium lacks a roof enürely.
(posterior) and preoptic (anterior) root, unite the trabe- The auditory capsule is parücularly poorly developed
cula with a slim dorsolateral rod, the orbital cartilage (taenia in caecilians, having large gaps in its walls. Tríese rep-
marginalis), thus forming the scant side wall of the chon- resent the fenestra ovalis (lateral), basicapsular fanestra
 Larvae
(ventral), and the perilymphatíc, endolymphatic, and more or less contemporaneously, the upper jaw (with 147
acousüc foramina (medial). Internally, there are three mineralized teeth) forms. Endochondral ossification in-
slender septae for the semicircular cañáis. The fenestra volves the exoccipitals, basisphenoid, and quadrate at
ovalis contains a rodlike columella that attaches laterally this stage. At the same time, various investing bones ap-
with the posterior face of the quadrate. Functionally, an pear—frontals, parietals, palatines, squamosals, and, in
operculum is absent, although some individuáis (e.g., de the lower jaw, the splenial. In a 44.5-mm foetus, the
Beer, 1937; Ramaswami, 1948) claimed that the oper- orbitosphenoid has begun to ossify along with the par-
cular cartilage is incorporated into the próxima! stapes. asphenoid, vomer (prevomer), and pterygoid. Fusión of
In contrast to the rest of the chondrocranium, the nasal the palatine and maxilla has occurred in a 51.8-mm foe-
capsule is moderately well formed, although it lacks a tus. The last bones to appear are the septomaxilla and
roof (tectum nasi) and a cartilage (planum antorbitale) columella in a 54.5-mm foetus. Subsequent develop-
between the posterolateral wall, lamina orbitonasalis, and ment involves elaboration and fusions of bony cranial
the medial septum nasi that separates the olfactory or- elements.
gans. The anterior unión of the cranial trabeculae forms
a ventral trabecular, or internasal, píate. This bears a Branchial Arches. The hyobranchial skeleton of lar-
vertical, medial píate of cartilage, the septum nasi, that val caecilians is robust and chondrifies early with respect
extends anteriorly as the prenasal process. Lateral exten- to the rest of the skull (Fig. 6-7); de Beer (1937) sug-
sions from the ethmoid píate fuse with the side wall of gested that this precocious development was associated
the nasal capsule (planum termínale) to form the floor of with the hyobranchial skeleton's function in supporting
the nasal capsule (solum nasi) and the anterior borders the long external gills. The stout ceratohyals articúlate
of the choanae. The anterior wall of the nasal capsule is ventrally with a median basibranchial. The second me-
formed by the alary cartilage that arises from the antero- dian basibranchial unites ceratobranchial pairs I and II
lateral región of the septum nasi. Anterolateral continuity midventrally. Ceratobranchial pair III are fused midven-
between the alary cartilage and the planum termínale trally but separated from anterior hyobranchial elements.
(side wall) is affected by the oblique cartilage. Together, The fourth pair of ceratobranchials are rudimentary and
the alary and oblique cartilages form the medial and dor- articúlate distally with the third pair.
sal margins of the externa! naris. A ventral strut of carti-
lage (infranarial cartilage) that extends anteromedially from Axial Skeleton. The larval vertebral column is differ-
the side wall of the nasal capsule to the anteromedial entiated regionally, but the vertebrae are more homo-
córner of the septum nasi forms the ventral border of the geneous in their sizes and proportions than are those of
external naris. the adult caecilian (M. Wake, 1980c). Apparently this
The quadrate cartilage (palatoquadrate) bears various results from a differential growth partern in which rnid-
connections to the central chondrocranium. In the an- body vertebrae grow more rapidly than anterior and pos-
teroventral auditory región it is connected to the basitra- terior vertebrae. It is the midbody vertebrae and their
becular (basipterygoid) process by a ligament (¡chthy- associated ribs and muscles that are critical to the organ-
ophis) or a cartilaginous basal process (pterygoid process) ism's locomotor actívities (Gans, 1973a); therefore, it is
in Gegeneophis, Siphonops, and Hypogeophis. Dorsally, not surprising that these are the most fully developed in
the processus ascendans of the quadrate is attached to the actively swimming larvae.
the orbital cartilage by fibrous tissue, and a small otic
process projects toward the otic capsule and establishes Salamanders
a connection with the distal end of the columella. Ven- The larval structure of Necturus, Amphiuma, Crypto-
trally, the quadrate is united with Meckel's cartilage of branchus, Trituras, Salamandra, and Ambystoma are the
the lower jaw which characteristically bears a long re- best known (Francis, 1934; de Beer, 1937), but these
troarticular process. larvae are as morphologically diverse as the adult mor-
photypes into which they may metamorphose (see Chapter
Ossification Sequence of the Cranium. Among the 13). Consequently, it would be misleading to describe
significan! features of larval caecilians in contrast to larval the larval morphology of any one species as typical for
anurans and salamanders are the lack of a sclerotic car- the order as a whole.
tilage and the early onset of ossification; by the time
metamorphosis occurs, nearly the entire cartilaginous External Features. Although the general morphology
neurocranium has been replaced by bone. This probably of larval salamanders is similar to that of their adult coun-
is correlated with the reduced structure of the chondro- terparts, a number of features serve to distinguish the
cranium which would afford minimal protection and sup- larvae from the adults—smaller size, external gills, a tail
port. Based on Dermophis mexicanas (M. Wake, 1982), fin, distinctive larval dentition, a rudimentary tongue (Me
the ossification sequence is as follows. Elements of the more than a muscular thickening of the floor of the mouth
mandible (mentomeckelian bones, articular and angular that allows prey to be held and manipulated against the
components, and retroarticular process) appear first palatal dentition), and the presence of a scleral cartilage
(29-mm foetus). Subsequently (33-36-mm foeruses) and that disappears at metamorphosis. The shape of the head
LIFE HISTORY
148
Basibranchial I

Basibranchial II
ceratohyal
Ceratobranchial I

Ceratobranchial II
Ceratobranchíal II

Ceratobranchial IV

hypohyal
Basibranchial
Basíbranchial I
pars reuniens ceratohyal
Basibranchíal Hypobranchial I

hypohyal Basibranchial II
píate' Hypobranchial II

Ceratobranchial, Ceratobranchial I
Ceratobranchial II

Ceratobranchial III
Ceratobranchial II Ceratobranchial IV

Figure 6-7. Hyobranchial skeletons of amphibian larvae. A. Dorsal view of Ichthyophis glutinosas.
B. Ventral view of Rana temporaria. C. Corsal view of Salamandra salamandra. Redrawn from Gaupp
(1906).

is less angular owing to trie absence of parotoid glands, lage, the hypochordal commissure, and anteriorly by a
poorly developed jaw musculatura, and incompletely de- second narrow transverse carülaginous bar, the crista
veloped maxillary arcade. The nostrils are wide, immo- stellaris, which separates the anterior and posterior fe-
bile, and not disünctly elevated. The eyes lack lids, and nestrae (e.g., in Salamandra). In some species (e.g., Am-
the lens is convex and protuberant. Larval salamanders bystoma macu/atumj, the crista breaks down; thus, the
(except sirenids) possess four fully developed limbs and fenestrae are confluent and the chondrocranium virtually
begin to feed soon after hatching. floorless. In others (e.g., Triturus), the posterior chondro-
cranial floor is invaded by mesotic cartilage, and the pos-
Chondrocranium and Mandible. The carttlaginous terior fenestra thus is obliterated. Three stout dorsal ex-
cranium is robust, and although less fenestrate trian that tensions arise from each cranial trabecula and unite with
of caecilians (Fig. 6-6), it is more delicate than are anuran the dorsolateral orbital cartilage to form the sides of the
chondrocrania. Unlike frogs, the salamander chondro- braincase. The pila antotíca is the most posterior; the
cranium does not undergo extensive modifications at oculomotor foramen lies between it and the second dor-
metamorphosis; thus, the larval skull can be thought of sal extensión, the pila metoptica. The optic foramen sep-
as a well-developed cartilage framework from which the arates the pila metoptica and the preoptic root. The
adult skull arises by ossificatíon of carülaginous elements braincase is open dorsally. The immense frontoparietal
and deposition of dermal bones on their surfaces. The fenestra is margined posteriorly by a transverse bridge of
floor of the chondrocranium bears one or two extensive cartilage, the tectum synoticum, that unites the auditory
basicranial fenestrae. The anterior basicranial fenestra is capsules. The orbital cartílagos form the lateral margins,
invariably present and formed by the cranial trabeculae, and the tectum intérnasele the anterior border of the
which border it laterally and fuse anteriorly to form the frontoparietal fenestra.
transverse internasal píate—the anterior margin of the The auditory capsules, which flank the parachordal píate
fenestra. The posterior basicranial fenestra, if present, lies laterally and are connected dorsally by the tectum syn-
in the basal píate uniting the auditory capsules and is oticum, are well developed and lack the basicapsular fe-
defined posteriorly by a narrow transverse bar of carti- nestra typical of caecilians. The medial wall is chondrified
 Larvae
for the anterior and posterior acoustic foramina which the lateral ramus of the nasal branch of the pro- 149
and perilymphatic and endolymphaüc foramina. Lat- fundus nerve exits. The dorsum of the capsule is un-
•aly. the capsule wall is perforated by the fenestra ovalis, roofed, bearing the large fenestra dorsalis, which is sep-
«Éach in turn is occluded by a columella and, in most arated from the anterolateral fenestra narina by a slim
^ecies, an operculum. The relationships of the columella bridge of cartilage, the oblique cartilage; the fenestra na-
are the origin of the operculum are variable (de Beer, rina marks the position of the external naris and entrance
: 1537). The columella arises as an independen! píate of of the nasolacrimal duct to the nasal capsule. The fora-
earüage that partially or wholly occludes the fenestra ovalis men apicale lies anteromedial to the fenestra narina and
and may or may not fuse with its margin. A rod or stylus provides an exit for the medial ramus of the nasal branch
áevelops from the píate; the stylus projects anterodorsally of the profundus nerve.
fcom the lateral wall of the auditory capsule and bears The quadrate (palatoquadrate) articúlales ventrally with
ene of several relationships with elements of the suspen- Meckel's cartilage, which forms the cartilaginous frame-
atxy and visceral apparatus. In Necturus, there is a liga- work of the mandible. Otherwise, the quadrate is fused
«nentous attachment of the distal end of the columella to to the central chondrocranium at three or four positions.
ifae squamosal; during development, the attachment shifts Among primitive salamanders (e.g., Cryptobranchus and
z> the posterior surface of the quadrate. Ambystoma, Hynobius), the quadrate is connected to the braincase
Salamandra, and some plethodontíds are characterized by means of the ascending process that fuses with the
by a synchondrotic unión of the quadrate and columella, pila antotica, and to the auditory capsule by means of
«hereas Triturus lacks any connecüon. In neotenic taxa, the basitrabecular, or otic, process of the basal píate.
such as Cryptobranchus and Amphiuma, the columella Anteroventrally the quadrate develops the pterygoid
bears a ligamentous attachment to the squamosal or process that extends forward and fuses with the postero-
quadrate and the ceratohyal; none of these species has lateral wall (planum termínale) of the nasal capsule. The
an operculum. In those species that metamorphose, an process is absent in some salamanders (e.g., Necturus),
operculum arises in either of two ways, or by a combi- but present in most; however, in more advanced sala-
nation of both. It may chondrify in the membrane of the manders (e.g., ambystomatids), the pterygoid process
hind part of the fenestra ovalis and grow forward (e.g., projects forward and ends freely, lacking the connection
plethodontids), or it may origínate from the otic capsule to the nasal capsule typical of more primitive salaman-
<e.g., Hynobius). Kingsbury and Reed (1909) believed ders. The quadrate also may bear a synchondrotic or
that the operculum originated from the auditory wall pos- syndesmotic association with the columella, as discussed
teroventral to the columella, whereas Reinbach (1950) above.
suggested that it formed from cells liberated from the otic
capsule. At metamorphosis, the columella is united syn-
chondrotically with the lateral wall of the auditory cap- Ossif ication Sequence of the Cranium. There have
sule, and the operculum, located in the fenestra ovalis, been surprisingly few studies of the process of ossification
is a free cartilaginous disc that is connected to the su- in salamander crania—a mechanism that is so extraor^
prascapula of the pectoral girdle by the opercularis mus- dinary that it deserves more attention. The most com-
de. The internal ear initially bears cartilaginous septa for plete accounts are of Triturus vulgaris (Erdmann, 1933),
Ihe anterior, lateral, and posterior semicircular cañáis, but Salamandra salamandra (Stadtmüller, 1924), Ambys-
in later stages of development, the posterior septum dis- toma mexicanum (R. Keller, 1946), Ambystoma tex-
appears. anum (Bonebrake and Brandon, 1971), and Aneides lu-
Among amphibians, the nasal capsules of salamanders gubris (T. Wake et al., 1983). Aside from these few
are unique in not sharing a medial wall (i.e., the septum comprehensive studies, there is considerable anécdota!
nasi of caecilians and anurans). Instead, the ventral tra- information, much of which was summarized by de Beer
becular píate gives rise to two vertical components, each (1937) and Larsen (1963).
of which forms the anterior and medial walls of its re- The fully developed salamander larva has a skull less
spective nasal capsule; the intervening space is termed extensively ossified than that of a caecilian, but far better
the cavum intérnasele. Posteromedially, the two capsules developed than that of anuran larvae. Salamander larvae
are joined by a transverse píate of cartilage (planum pre- are unique in that the entire bony palate is remodeled at
cerebrale) that arises between the olfactory nerves. The metamorphosis, and in contrast to caecilians, the main
planum precerebrale, together with the planum antorbi- component of the upper jaw, the maxilla, does not ap-
tale (a lateral outgrowth of the trabecular píate), com- pear until late in larval development. Ossification com-
pletes the posterior and lateral walls of the nasal capsule. mences before larvae begin to feed, and is marked by
A small cartilaginous process (inferior prenasal process) the appearance of the vomers, palatines, dentaries, co-
protrudes anteromedially (against the overlying premax- ronoids (splenials), and premaxillae—all of which bear
illary bone) from the anteromedial wall of each capsule. simple, conelike larval teeth. The parasphenoid, preartic-
The capsule thus formed is rigid but fenestrate. The large ulars, squamosals, and precursors of the pterygoids ap-
ventral fenestra choanalis endoses the internal choana. pear at a time approximately coincident with the opening
The side wall bears the large fenestra lateralis through of the larval mouth. The prearticular, coronoid, and den-
LIFE HISTORY
150 tary invest Meckel's cartilage to form the mandible. The controls the opening and closing of the gilí slits. As de-
maxillary arch is abbreviated, being composed of only scribed by Severtzov (1968), the floor of the buccal cavity
the premaxillae (or a fused premaxillary complex). The is depressed at the same tíme that the mouth is opened
palatal bones (vomers and palatines) form longitudinally and the gilí arches are closed. This forces a stream of
oriented dental arcades that laterally flank the para- water (along with prey) into the mouth. Closure of the
sphenoid, which forms a floor to the fenestrate chondro- mouth and lifdng of the floor of the buccal cavity forces
cranial braincase. This configuration of elements forming most of the ingested water out through the gilí slit as it
the jaws and palate allows the larva to open its mouth opens. When the gilí slit closes and as the floor of the
rapidly and to suck in prey. Once in the buccal cavity, buccal cavity continúes to be elevated, the increasing
prey can be adpressed against the palate by the rudi- pressure forces the contents of the buccal cavity to the
mentary tongue, and swallowed. esophagus where it is swallowed.
Subsequent to the appearance of bones involved in
larval feeding, the major dermal roofing bones—the fron- Axial Skeleton. There are limited ontogenetic data
tals and parietals—begin to ossify. These are followed by on the postcranial anatomy of salamanders and no stud-
endochondral ossifications of the chondrocranium rep- ies similar to that on caecilians by M. Wake (1980c).
resenüng the paircd exoccipitals, prootics, opisthotícs, Apparently, most workers (except T. Wake et al., 1983)
quadrates, and the orbitosphenoid (sphenethmoid), and have assumed like I. Wilder (1925:92) that postcranial
the initial appearance of the maxilla. Generally, the last elements in general and the appendicular skeleton in par-
elements to ossify in the larvae are the columella and ticular of larval salamanders are unimportant because
various dermal elements that occur spuriously in sala- "larval appendages are examples of adult characters which
manders—namely, prefrontals, lacrimáis, nasals, septo- make an anachronistic appearance."
maxillae, and quadratojugals.
Anurans
Branchial Arches. The hyobranchial skeleton of sal- Of the three orders of amphibians, anuran larvae are the
amander larvae is a good deal more complicated than most deviant from their adult counterparts and the most
that of caecilians (Fig. 6-7), owing to its role in food specialized of the three larval types. Moreover, among
capture by the carnivorous larvae. Although there is con- those anurans having free-swimming larvae, there is an
siderable variation in the structure of the skeletal unit, in astounding array of morphological variation relative to
the fully formed larva the hyobranchial apparatus basi- that observed in either caecilians or salamanders. This
cally consists of a median basibranchial series of one or diversity is related to several evolutionary phenomena.
two elements. If two elements are present, the anterior Morphologically, anurans are more specialized than sal-
basibranchial is the larger, and the posterior is a slim rod amanders (and specialized in a different way than cae-
of cartilage. When only one element is present, it usually cilians)—that is, their body plan has deviated the most
bears a posterior projection, suggesting that the two cop- strikingly from the short-limbed attenuate body plan of
ular elements have fused to form one píate. The anterior the more generalized, and presumed primitive, ancestral
margin of the hyobranchial apparatus is composed of the form. They alone are capable of saltatorial movement
anterior tip of the basibranchial that is flanked laterally between and within terrestrial and aquatic habitáis. This
by small hypohyal and large ceratohyal elements. To- is facilitated, of course, by their long hindlimbs and short
gether, these components form a broad carülaginous are trunk. Thus, it is not surprising that their larvae deviate
that comes to rest against the lower jaw when the hyo- from the generalized morphological and developmental
branchial apparatus is protracted during feeding. mode observed in the other orders. Anurans have under-
The larger of the basibranchial plates (if two are present) gone phylogenetic and ecological diversificaüon that far
bears two pairs of posterolateral processes, Hypobran- surpasses that observed in salamanders and caecilians;
chials I and II (Branchial Arches I and II). The first pair anuran larvae reflect this diversification and differ strik-
usually is fused to the basibranchial, whereas the second ingly from their adult counterparts in their habits, ecol-
pair normally articúlales with it. Distal to the hypobran- ogy, and morphology. Because of this complexity it is
chials are three or four pairs of ceratobranchials (termed exceedingly difficult to draft a "generalized" account of
epibranchials by some authors). Ceratobranchials I and anuran larvae comparable to that presented for caecilians
II articúlate with the distal ends of Hypobranchials I and and salamanders. Consequently, this section is organized
II, respectively. In turn, the ceratobranchials are united on a slightly different scheme than the preceding ones.
to one another proximally and distally by delicate carti- A general morphological account of the body plan and
laginous connections. chondrocranial, visceral, and axial elements is provided
The entire apparatus bears a ligamentous connection before accounts of basic types of anuran larvae, with
to the skull. The complexity of its design accommodates details of the buccopharyngeal morphology and the func-
movement in the dorsoventral and anteroposterior planes tional interrelationships of feeding and respiration.
as well as a certain degree of rotation around the longi-
tudinal axis. Movement of the hyobranchial skeleton Basic Body Plan. At hatching, a tadpole seems to
changes the volume of the oropharyngeal cavity and resemble a fish. However, this superficial similarity belies
 Larvae
ariking differences. The body is short (approximately than a vertical position, and the anterior chondrocranial 151
25-35% of the total length) and generally ovoid. The cartilages are modifed to form structural support for the
tong tail is laterally compressed and composed of a cen- tadpole mouth. During metamorphosis, these parts of the
ital axis of caudal musculatura provided with dorsal and chondrocranium are restructured and repositioned totally
wentral "fins." The ventral fin is continuous from the vent to provide for the mandibulae and suspensory apparatus
at the posterior end of the body to the üp of the tail. The of the adult—an architectural system similar to that of
dotsal fin extends from the top or end of the body to the adult and larval salamanders and caecilians.
ip of the tail. The unión of dorsal and ventral fins distally The floor of the anuran chondrocranium bears one
assumes a variety of terminal shapes depending on the relatively small fenestra, the basicranial fenestra, which is
acaptive type of the larva. Similarly, the shapes and sizes bordered laterally by the cranial trabeculae and anteriorly
of the dorsal and ventral fins vary. by the trabecular píate. Posterior to the fenestra, the floor
The body of the tadpole is characterized by slightly of the chondrocranium is composed of a broad sheet of
protuberant, lidless eyes, wide nares, and a terminal mouth, cartilage, the basal píate. From this ventral framework
which is highly variable in form and posiüon. In its most three pillars of cartilage extend dorsally to form the sides
amplistic state (e.g., pipoids), the mouth is wide and slit- of the braincase. The most posterior is the pila antotica,
&e. Most anuran larvae have more complex mouths which fuses with the roof of the otic capsule dorsally,
eharacterized by fleshy, papillose or funnel-shaped "lips." thereby forming the prootic foramen through which the
fcitemal to the lips, the mouth usually bears rows of fine, trigeminal, facial, and abducens nerves exit the chondro-
seratinous denudes and a prominent beak, beyond which cranium. A second strut of cartilage, the pila metoptica,
les the buccopharyngeal cavity. Although absent in most lies anterior to the pila antotica. Fusión of these two pilae
anuran larvae, sensory barbéis border the mouth in some dorsally endoses the foramen for the oculomotor nerve
ptpoid larvae. Early in development, anuran larvae have and opthalmica magna artery. The optic and trochlear
extemal gills, anterior to which lies a fold of skin. The nerves emerge between the pila metoptica and a third,
opercular fold grows posteriad to endose the gills in all more anterior pillar of cartilage, the preoptic root, which
amphibians that metamorphose; however, this occurs forms the anterior comer of the braincase. A fourth set
much earlier in the development of anurans than in sal- of cartilage pillars, the pilae ethmoidalis, arise from the
amanders and caecilians. Thus, in young anuran larvae, anterior floor of the chondrocranium to form the anterior
the gills come to be enclosed in an opercular chamber wall of the braincase (Fig. 6-4). This wall has a medial
ihat opens to the outside vía a funnel-shaped spiracle or fenestra between the pilae ethmoidalis, the fenestra pre-
pair of spiracles. The position and number (one or two) cerebralis, and a pair of anterolateral foramina, the for-
of spiracles vary depending on the species. amen olfactorium, formed between the pila ethmoidalis
Whereas larval salamanders are characterized by func- and the preoptic root. The olfactory nerve exits the brain-
tional fore- and hindlimbs, anuran larvae are not. The case via the foramen olfactorium. The fenestra precere-
forelimbs develop within the opercular chamber and erupt bralis is obliterated in early metamorphosis by the de-
through the body wall just prior to the completion of velopment of a medial septum that extends anteriorly to
metamorphosis. The hindlimbs first appear as buds that sepárate the nasal capsules and provide a complete an-
emerge from the posterior margin of the body and de- teromedial wall to the braincase. The dorsal ends of the
velop adpressed to the tail. Thus, throughout its larval lateral pilae are united by the orbital cartilages, and the
ufe, the tadpole maintains a hydrodynamically efficient, anterior pilae are joined dorsally by the tectum interna-
fusiform shape, with the limbs becoming functiona! only sale. Together, these cartilages form the anterolateral and
toward the completion of metamorphosis when the or- anterior margins, respectively, of the frontoparietal fe-
ganism moves from an aquatic to a terrestrial environ- nestra in the roof of the braincase.
ment. Dorsal fenestration of the anuran chondrocranium is
In contrast to salamanders and caecilians, the digestive variable, depending on the degree of development of the
system of anuran larvae is strikingly different from that roofs of the auditory capsules. If the auditory capsules
of the adults. Owing to the microphagous, herbivorous are united only by a single, posterior bridge, the tectum
food habits of most anuran larvae, they require a large synoticum, then the frontoparietal fenestra is extensive.
intestinal surface área for absorbing nutrients; thus, the If the capsules are united anteriorly by the taenia tecti
intestino is long and coiled on itself. The stomach is un- transversalis, as well as posteriorly, the dorsal fenestration
developed, but near the cardiac portion of the presump- is subdivided into the anterior frontoparietal fenestra sep-
tive stomach is a structure known as the manicorto gland; arated from the posterior parietal fenestra by the taenia
presumably secretíons of this gland aid in the digestión tecti transversalis. Occasionally the latter is developed in-
of food. completely, thereby effecting only partial separation be-
tween the fenestrae. Appearance of a dorsomedial (i.e.,
Chondrocranium and Mandible. Contrasted to the longitudinal) bridge of cartilage, the taenia tecti medialis,
chondrocrania of salamanders and caecilians, that of between the taenia tecti transversalis and tectum syno-
anurans is robust and boxlike (Fig. 6-6). Fenestration is ticum subdivides the posterior parietal fenestra into two
reduced. The palatoquadrate lies in a horizontal rather smaller fenestrae.
LIFE HISTORY
152 Jhe auditory capsules flank the posterior floor of the erally, the palatoquadrate bears a dorsal process, the pro-
braincase; thus, their ventral aspect is complete. In this cessus muscularis quadraü, from which the depressor
respect anurans and salamanders are alike and differ from muscles origínate; these muscles insert on the ceratohyal
caecilians, which have a basicapsular fenestra. In contras! ventrolaterally.
to salamanders and caecilians, each of which lacks the
taenia tecti transversalis and taenia tecti medialis, the au- Ossification Sequence of the Cranium. Owing to
ditory capsules of anurans tend to be roofed more com- the dramatic structural and functional changes in the anu-
pletely. The lateral wall of the auditory capsule has an ran skull at metamorphosis, cranial ossification is delayed
opening, the fenestra ovalis. Associated with this fenestra for the most part unül the onset of metamorphosis. A
is a píate of carülage, the operculum, that occludes the discussion of these aspects of development follows in
posterior part of the opening. A second cartilage, the Chapter 7.
rodlike stapes, or columella, arises independently of the
auditory capsule, but fuses with its ventral margin and Branchial Arches. There is considerable diversity
has ligamentous attachments to the quadrate anterolat- among anurans in the structure of their branchial appa-
erally and the operculum posteriorly. The medial wall of ratus, but basically each consiste of a pair of robust an-
the auditory capsule is perforated by one to three acous- terior plates, the ceratohyals, that underlie the floor of
tíc foramina and two perilymphatic foramina (superior the buccal cavity and that usually unite ventromedially
and inferior). The posteromedial wall of the auditory cap- to one another (Fig. 6-7). Anterolaterally the ceratohyals
sule is completed by the occipital arch of the posterior articúlate with the palatoquadrate, and posteromedially
end of the chondrocranium. The unión of these two they are fused to a basibranchial cartilage. Presumably
structures accommodates two foramina, the posterior the latter is homologous with the second basibranchial of
jugular foramen through which the glossopharyngeal and salamanders and caecilians, the first basibranchial having
vagus nerves exit the cranium, and a third perilymphatic been lost or reduced in anurans. The basibranchial artic-
foramen. úlales posteriorly with two broad cartilages, the hypo-
The anterior end of the chondrocranium of anurans is branchial plates, from which four ceratobranchials arise
unlike that of salamanders and caecilians. The nasal cap- on each side. The ceratobranchials are united distally,
sules characterisric of the latter organisms do not develop forming a basketlike framework which supports the larval
in anurans until metamorphosis owing to the structure gilí filters. The structure of the larval branchial apparatus
and function of the larval mouthparts and their role in is associated intimately with buccal pumping and feeding
larval respiraüon. With the excepüon of microhylids in mechanisms described below. With the shift in feeding
which the nares do not open until just before metamor- mechanisms at metamorphosis, the branchial apparatus
phosis, the external nares of tadpoles remain open per- undergoes profound modifications to form the adult hyoid
manently and communicate with the internal nares by apparatus, which supports the laryngeal structures and
means of a short passage through the buccal roof; parts serves as a base for the tongue.
of the passage are lined by olfactory epithelium, but a
discrete olfactory organ does not develop until meta- Morphological Types of Anuran Larvae. Orton
morphosis. (1953) recognized four basic kinds of tadpoles, which she
The floor (planum trabeculae anterior) of the anterior designated as Types I-IV depending on the structure of
end of the braincase bears a pair of anterolateral projec- the opercular chamber and its opening(s) from the body,
üons, or cornua. Each cornu is deflected ventrally and and the nature of the larval mouth (Fig. 6-8). Type I
fused anteriorly with the suprarostral cartilage, which includes the peculiar pipids and rhinophrynids that have
supports the upper beak of the larva. Posterolaterally, paired spiracles (one opening from each of two spiracular
the cornua bear a ligamentous connection (quadrato- chambers), that lack keratinous mouthparts, and some
cranialis ligament) with the anteromedial margin of the of which possess sensory barbéis bordering the simple,
quadrate cartilage. The lower beak is supported by paired, slitlike mouth. A single family, the Microhylidae, is rep-
medial chondrifications, the infrarostrals. Medially, these resented in Orton's Type II tadpoles. Like Type I larvae,
elemente articúlate with one another; posterolaterally each Type II tadpoles lack mouthparts. They also lack barbéis
articúlales with Meckel's cartilages. The latter, in turn, and have a single opercular chamber with a single, me-
articúlate laterally with the palatoquadrate. The palato- dian posterior spiracle. Types III and IV larvae have
quadrate is massive and aligned horizontally in lateral mouthparts. Orton distinguished Type III larvae (asca-
view, and lateral and parallel to the neurocranium in dor- phids and discoglossids) from Type IV larvae (all remain-
sal view. Posteriorly, it is connected to the pila antotíca ing families) on the basis of the midventral spiracle in the
via the ascending process of the quadrate and to the former and the sinistral spiracle of the latter.
auditory capsule via the larval otic process. Anteriorly, As originally proposed, Orton's scheme was phenetic
the processus quadrato ethmoidalis forms a massive strut and provided a convenient, shorthand way of classifying
between the anterolateral córner of the neurocranium tadpole morphotypes. Subsequent workers sought to ar-
and the anterior end of the palatoquadrate. Anterolat- range these types in a phylogenetic sequence. Thus, P.
 Larvae
153

Figure 6-8. Morphological types of

anuran larvac; mouths and ventral
views of bodies showing positions of
spiracular openings. A—D. Orton's
(1953) types 1-4, respectively.
E. Otophryne robusta.

Starett (1973) elaborated Orton's work and proposed anterior filter valve of the buccopharyngeal cavity is un-
•ames for the morphological types, and the ñames were paired, extending across the glottis in the midline.
appfied to suborders of frogs by some workers (e.g., Type III tadpoles are characterized by a "high" sus-
i Savage, 1973). As more recent research (Sokol, 1975) pensorium similar to that of salamander larvae and dif-
las shown, Orton's classif¡catión is vastly oversimplified. fering from the "low" suspensoria of other tadpoles (So-
Moreover, ontogenetic studies suggest the possibility of kol, 1975). The suspensorium involves the structures that
"*primitive" types of tadpoles (Types I and II) being de- suspend the main portíon of the palatoquadrate from, or
•wed through developmental truncation from "ad- attached to, the braincase. In tadpoles having a "high"
«nced" types (Types III and IV) (Wassersug, 1984; suspensorium, the anterior end of the palatoquadrate is
Wassersug and Duellman, 1984). The types, as defined deflected ventrally, whereas in those having a "low" sus-
below, still provide a useful framework within which to pensorium, the long axis of the palatoquadrate is nearly
describe tadpoles, but too little is known about the dis- level owing to the attachment of the posterior end of the
Mbution and variation of the characters within and be- lower aspects of the braincase. In Type III tadpoles, the
*een types to warrant a phylogeneüc assessment. ascending process of the palatoquadrate fuses to the neu-
Type III tadpoles.—This type was termed the Lem- rocranium at the dorsal end of the pila antotica (the dor-
manura by P. Starrett (1973) and Discoglossoidea by sal column of cartilage that sepárales the oculomotor and
Sokol (1975). There are a number of features of ascaphid trigeminal foramina just in front of the auditory capsule).
and discoglossid tadpoles that seem to be primitive. The A second process of the palatoquadrate, the otic process,
tedpoles have a shallow opercular chamber similar to that bears a ligamentous attachment to the anterior end of
of salamanders. The chamber is provided with a single, the auditory, or otic, capsule. In tadpoles having a "high"
midventral opening to the exterior. This opening, or spir- suspensorium, the anteromedial margin of the dorsal as-
acle, is formed by a single hiatus in the fusión of the pect of the oüc capsule bears a projecting shelf or ledge
opercular skin to the body wall; thus, a siphon is absent. that connects the otic capsule with the taenia tecti mar-
So far as is known, Type III tadpoles are unique among ginalis. This ledge overlies the upper end of the ascending
anurans in having sepárate trigeminal and facial ganglia process.
(C.N. V and VIH), a condiüon characteristic of salaman- Other morphological complexes of Type III larvae are
ders (Sokol, 1975). Branches of these nerves exit the perceived as showing one or more derived features (So-
cranium through the prootic foramen and the palatine kol, 1975). For example, in the hyobranchial apparatus,
foramen, which are separated by a bar of cartilage, the the branchial basket is composed of two complete septa
prefacial commissure. The palatine foramen and henee and a third, incomplete septum. A septum is defined as
the prefacial commissure are absent in all other tadpoles. the aortic arch complex (afferent and efferent vessels),
Type III tadpoles possess a shearing beak and rows of an interbranchialis muscle, and the surrounding tissues
keratinous denudes. Internal gills are present, and the associated with each ceratobranchial and its internal gills.
LIFE HISTORY
154 Type III tadpoles lack the third interbranchialis muscle. cending process of the palatoquadrate extends lateral to
In salamanders, the ceratobranchials bear a ligamentous the palatoquadrate from the ventral margin of the neu-
attachment to the hypohyals. Similarly, in some Type III rocranium (the región of the cranial trabecula).
tadpoles, the ceratohyals have a ligmentous connectíon A host of derived features characterize Type II larvae.
to the hypohyal píate; this presumably represents a de- These include the two that are shared with Type III and/
rived condition from the primitíve ligamentous connec- or Type IV tadpoles: (1) presence of a single prootic
tion between these elements in salamanders and some ganglion and loss of the palatine foramen and prefacial
other tadpoles. commissure; (2) fusión of ceratohyal and hypohyal ele-
Type IV tadpoles.—This is the Acosmanura of P. Star- ments; (3) fusión of the second basibranchial with the
rett (1973) and the Ranoidea of Sokol (1975). Type IV hypohyal píate. They are distinguished from Type III and
tadpoles include the majority of anurans—all except the IV larvae by the presence of a paired anterior filter valve
ascaphids, discoglossids, microhylids, pipids, and rhino- and glottis that is displaced anteriorly. The opercular
phrynids. They show fewer primitive features than do chamber is greatly enlarged and bears a single spiracle
Type III larvae, but nonetheless are characterized by a with a siphon. In all known microhylids except Oto-
melange of primitive and derived characters. Like Type phryne robusta (Fig. 6-8E) and Pseudohemisus granu-
III larvae, Type IV tadpoles possess a shearing beak and losum, the spiracle is midventral and located beneath the
usually rows of keratinous denudes. Interna! gills are vent. Similarly, all microhylids except O. robusta and
present, and the anterior filter valve of the buccophar- P. granuhsum lack keratinous mouthparts. In O. robusta,
yngeal cavity is unpaired. In contras! to Type III tadpoles, the mouth is simple and lacking oral papillae like those
the branchial basket is composed of three complete septa, of other microhylids; however, O. robusta has a single
and the attachment between the second basibranchial row of sharp, fanglike, cornified "teeth" along the upper
and the hypohyal píate is ligamentous. The ceratobran- and lower jaws (Fig. 6-9) (Pybum, 1980b). These "teeth"
chials are ligamentously attached to the hypohyal píate are not homologous with true teeth and are unique in-
in some Type IV tadpoles and fused in others. sofar as is known; no one has speculated as to their
The suspensoria of Type IV tadpoles generally are possible homology with the denticular structures of Type
"lower" than those of Type III larvae because the oüc III and IV larvae. The spiracle of O. robusta also is bizarre.
process lies posteroventral to the most anterior margin of The opercular chamber is enlarged, and the spiracle is
the otic capsule; thus, the palatoquadrate lies in a plañe posterior, as is typical of microhylids, but the spiracle is
almost paralleling that of the floor of the neurocranium. sinistral instead of midventral, and the siphon is elon-
The ascending process of the palatoquadrate either slopes gated into an enormously attenuate tube that extends
downward toward the otic process from its point of fusión from the body caudad about half the length of the tail.
with the dorsum of the pila antotica or, in the absence Type I tadpoles.—This is the Xenoanura of P. Starrett
or reduction of the pila antotica, extends in a lateral plañe (1973) and Pipoidea of Sokol (1975). All features used
from the wall of the neurocranium to the palatoquadrate. to distinguish the Type I pipid and rhinophrynid tadpoles
Type IV tadpoles lack an otic ledge or shelf connecting from Type II, III, and IV larvae seem to be derived. The
the otic capsule to the taenia tecti marginalis. opercular chamber is shallow and divided into two parts
Other, apparently derived features of Type IV larvae of reduced size. Each chamber bears a ventral and hiatal
include the following. The opercular chamber is deep and opening; thus, the spiracles are said to be paired and
provided with a single spiracle with a tubular siphon lacking siphons. The trigeminal and facial ganglia are fused,
opening to the exterior. Secretory tissue in the branchial so Type I tadpoles lack a palatine foramen and prefacial
food traps is organized into ridges. The spiracle is sinistral commissure. The mouth bears neither a beak ñor kera-
in all Type IV tadpoles, except in the larvae of F/ecton- tinous denudes. Internal gills are absent, and the anterior
oíus and Frítziana, two genera of egg-brooding hylids in filter valve of the buccopharyngeal cavity is paired with
which the spiracle is midventral (Griffiths and Carvalho, a median hiatus. The branchial basket of the hyobran-
1965; Duellman and Gray, 1983). The trigeminal and chial apparatus is composed of only two complete septa;
facial ganglia are fused; thus, the palatine foramen and thus, the third interbranchialis muscle and aortic arch
prefacial commissure are absent. complex are absent. The ceratohyals are reduced in
Type II tadpoles.—This is the Scoptanura of P. Star- number and fused to the hypohyal píate in Hymenochi-
rett (1973) and the Microhyloidea of Sokol (1975). Type rus and Pseudhymenochirus. The second basibranchial
II tadpoles include only a single family, the Microhylidae, is fused to the hypohyal píate.
which is characterized by only two primitive features. Like The suspensorium of Type I tadpoles is "high," but
Type III and IV larvae, the microhylids have internal gills, structured in such a way that it bears little resemblance
and like Type IV tadpoles, they have branchial baskets to the "high" suspensorium of Type III larvae and sala-
composed of three complete septa. manders. Because the palatoquadrate is short, its otic
The suspensorium is "low" because the otic process process does not reach the anterior end of the otic cap-
is fused with an extensión of the crista parotica of the sule. The ascending process of the palatoquadrate at-
otic capsule. The pila antotica is absent; thus, the as- taches to the dorsal end of the pila antotica but is not
 Larvae
155

Figure 6-9. Part of the mouth of the

tadpole of Otophryne robusta. The
sharp "denticles" are on the margin
of the upper jaw; "denticles" on the
margin of the lower jaw are obscured
by a fleshy fold. Note the shedding of
the outer ¡ayer of the third "denticle"
from the left. Scanning electrón
micrograph by W. R. Fagerberg
provided by W. F. Pyburn.

owerlain by an otic ledge of the auditory capsule, because of the mouth circumdistal to the beak. The larvae use
4iat structure is absent. Furthermore, the gap between their jaws and these keratinous structures to chop food
1he ascending and otic processes is filled by a cartilagi- into sizes that can pass through the small gape of the
nous píate that is fused to the otic capsule. The nerves mouth and/or to scrape or rasp food from surfaces. The
Iramus mandibulomaxillaris of the trigeminal and ramus mouth also acts as a valve in a buccal-pump system in
ophthalnnicus of the facial) that pass behind the ascend- which water flows into the buccal cavity via the oral ap-
ing process pierce the otic píate through two foramina. erture, caudally to the pharyngeal cavity, and trien over
the gills in the branchial baskets to emerge to the exterior
Functional Interrelationships Between Respira- via the spiracle(s). Simultaneously, food particles are
tory and Feeding Mechanisms. Two major distinc- trapped and gases are exchanged from this flow of
tions between anuran larvae and those of caecilians and water.
salamanders are the presence of internal gills and spe- The morphological components of the buccal pump
cialized larval mouthparts lacking true teeth in tadpoles. system consist of two internal chambers—the buccal and
It is implicitly clear from their morphology that anuran pharyngeal cavities—through which water flow is con-
larvae, unlike the larvae of the other orders, must have trolled by three valves—the mouth, as described above,
evolved mechanisms for (1) irrigating their internal gills, aided by the choanae and ventral velum. Each choana
and (2) obtaining food in the absence of jaws provided has a flaplike, semilunar valve of the mucosa along its
with teeth that, together, act to grasp and manipúlate posterior borden During aqueous ventilation, hydrostatic
food. The processes are related functionally and are de- pressure inside the buccal cavity closes the valve, thereby
pendent on a complex morphological system that is re- preventing a backflow of water through the nasal cham-
structured completely at metamorphosis. ber (Gradwell, 1969). The ventral velum is an epithelial
The tadpole mouth, or opening to the buccal cavity, flap that arises from the floor of the buccal cavity and
is supported by three cartilaginous elements. Dorsally there separates this chamber from the more posterior branchial
is a suprarostral cartilage that pivots on the ends of the baskets of the pharynx. A ventral velum is possessed by
cranial trabeculae, and ventrally the paired infrarostrals all anuran larvae except pipids. In this family, backflow
that articúlate with the distal ends of Meckel's cartilages. of water is prevented by flaplike covers of the paired
A complex set of ligaments and visceral musculature opercular openings (Gradwell, 1971). The final morpho-
(Gradwell, 1972a, 1972b) effects movement of these la- logical component of this system is the larval hyobran-
bial cartilages through movement of the larval hyoid. In chial apparatus and its associated musculature. Depres-
all anuran larvae, except microhylids and pipoids, the sion of the ceratohyals results in expansión of the buccal
mouth is provided with a keratinous beak (supported by cavity; thus, water flows through the mouth and nares
labial cartilages) and various configurations of rows of into the buccal cavity. When the medial portions of the
keratinous denticles and labial papillae on the fleshy área ceratohyals are elevated and the mouth closes, the buccal
LIFE HISTORY
156 cavity is contracted, the choanae closed by hydrostaüc at hatching have external gills that are resorbed within a
pressure, and the water forced from the buccal cavity few days. Their eel-like locomotíon is in quiet water or
over the ventral velum and into the branchial baskets of in mud. Essentially there are no adaptíve modificatíons
the pharynx. ContracrJon of the branchial baskets drives of the larvae, which are distínguished from adults pri-
the water through the gilí slits and then out via the spir- marily by having an open gilí slit and a better-developed
acle or opercular opening. Details of this mechanism are lateral-line system.
given by De Jongh (1968), Kenny (1969b), Gradwell
(1968, 1970, 1972a, 1972b), Severtzov (1969), and Salamanders
Wassersug and K. Hoff (1979). Three adaptíve types of salamander larvae are recog-
As anuran larvae pump water through their bucco- nized (Valentíne and Dennis, 1964). These types have
pharyngeal cavitíes, they extract food partícles suspended differences in their gills, in opercular covers (Fig. 6-10),
in the water. Their ability to do so depends on the pres- and in the degree of development of caudal fins. In gen-
ence of secretory epithelium and on the configuration of eral, larvae that develop in quiet water have laterally
the buccal cavity, which bears species-specific configu- compressed bodies, high caudal fins, balancers, and large
rations of papillae (Wassersug, 1976, 1980). Food par- gills, as contrasted with larvae that develop in streams.
tícles that are small enough to enter the mouth are sorted The size and surface área of the gills are dependen!
mechanically in the buccal cavity. Larger párteles are on the oxygen content of the water. Furthermore, ob-
shunted directly posterior into the esophagus, whereas servatíons and experiments suggest that the large bushy
smaller partícles move over the ventral velum into the gills in pond-type larvae are important in respiratíon at
pharynx. There, the larger of these small partícles are higher temperatures, at which time the oxygen content
trapped by direct interception and inertial impacüon on of the water is low, and also at times of activity (Whitford
the gilí filters and smaller párteles are aggregated in mu- and R. Sherman, 1968; Guimond and V. Hutchinson,
cus on the branchial food traps (Kenny, 1969b; Wasser- 1972). Extensive surface área of the gills increases res-
sug, 1972, 1980). Aggregates of small párteles of food piratory efficiency in water with low oxygen content and
are moved posterolaterally from the gilí filters to the cil- thereby enables these salamanders to survive in stagnant
iary groove that marks the margin of the roof of the ponds—a habitat occupied by many kinds of pond larvae
pharynx on each side. Once in the ciliary groove, food (Fig. 6-11). Stream larvae, on the other hand, live in cool
is transported posteriorly to the esophagus. Food is en- water with a high oxygen content; probably much of their
trapped and aggregated by mucous strands produced by respiration is cutaneous. The atrophied gills of the moun-
zones of specialized epithelium (Kenny, 1969c). A zone tain brook-type of larvae are indicative of primarily cu-
of pitted, secretory epithelium is present as a transverso, taneous respiratíon. The small gills in such species also
crescentíc band at the posterior margin of the buccal roof, allow these salamanders to crawl into underwater cracks
and often along the posterior edge of the ventral velum and crevices.
(Wassersug, 1976). A second kind of secretory epithe- The extent of the caudal fin and lateral compression
lium, ridged epithelium, forms secretory ridges on the of the body and tail are correlated with the nature of the
ventral surface of the ventral velum. From the velum, the larval habitat. Pond-dwelling larvae walk about on the
ridged epithelium may extend ventrally into each filter bottom of ponds, but at least some of them commonly
chamber to form branchial food traps. feed near the surface at night (J. D. Anderson and Graham,
1967), at which time they maintain their positíons and
move about by gentle movements of their thin but deep
ADAPTIVE TYPES OF LARVAE tails. Moreover, the deep tails are effectíve in rapid ac-
Many of the structural differences among larvae in the celeratíon in quiet water, when the larvae are disturbed.
three groups of living amphibians are associated with the Proportonately more muscular tails with shallower and
different environments in which they live. These differ- less extensive fins are characteristíc of larvae that develop
ences may not be correlated with the systematíc relatíon- in streams. Locomotíon in streams is accomplished pri-
ships of the taxa. Similar selective pressures on larvae of marily by crawling on the substrato. The tail may be used
diverse phylogenetic lineages has resulted in many ex- for balance or for short bursts of swimming, and if move-
amples of convergence of morphological features in lar- ment is against the current, the strong musculature and
vae of unrelated taxa in similar habitáis. Conversely, en- shallow fleshy fins are more effective in propulsión than
tírely different adapüve types of larvae exist among closely the deeper but comparatively weak tails of pond-type
related taxa. larvae. Caudal fins are reduced further in mountain brook-
In salamanders the major structural differences are as- type larvae; these move almost exclusively by crawling.
sociated with respiratíon and locomotíon, whereas among The surface área of the caudal fins also may be important
anurans the adaptatíons seem to be associated with feed- in respiration; thus, the increased surface área of the tails
ing and locomotion (or maintaining their positíon in the of larvae in ponds facilitates cutaneous respiration. Re-
environment). Free-living larvae of ichthyophiid and duced fins in stream-dwelling larvae may facilítate their
rhinatrematid caecilians have slight fins on their tails and taking refuge in crevices.
 Larvae
157

Figure 6-10. Adaptive types of

salamander larvae. A. Pond type—
Ambystoma tigrinum, with large
bushy gills and high caudal fin.
B. Stream type—Gyrínophilus
porphyríticus, with shorter, less
filamentous gills and low, fleshy
caudal fin. C. Mountain brook type—
Rhyacotriton olympicus, with short,
stubby gills and reduced caudal fin.

Figure 6-11. Pond larva of

Ambystoma opacum from
Centreville, Virginia. The large,
filamentous gills provide extensive
respiratory surfaces for survival in
ponds with low oxygen content.
Photo by K. Nemuras.

Balancers are paired, rodlike lateral projections that type larvae hatch with well-developed forelimbs and lack
develop on the head of many pond-type larvae (Fig. balancers, Salamandrina has rudimentary balancers.
5-12). In some species they are resorbed before the lar- The three adaptive types of salamander larvae are de-
vae hatch. In others they persist until the developing fore- fined as follows.
limbs have become fully funcüonal. During this interim, Pond-type larvae have an operculum forming a guiar
the balancers (along with the extended forelimbs) seem fold that is deeply incised midventrally (Fig. 6-10A). The
to keep the larva from sinking into the muddy substrate gilí rami are long and tapering, and each ramus has two
and help the larva to maintain its balance during its first, rows of long fimbriae with many other fimbriae intercol-
feeble attempts at locomoüon using the forelimbs. The lated between the rows. Gilí rakers, long conical projec-

r
absence of balancers in some pond-type larvae (e.g., sir- tions on the inner surface of the rami, are present. Bal-
enids) is unexplained at present. Although most stream- ancers usually are present in early larval stages (absent
LIFE HISTORY
158 ¡n some Hynobius and Tarícha, and rudimentary in Sal- and tapering, and each ramus bears two rows of mod-
amandra and plethodontids). The dorsal and ventral cau- erately long fimbriae. Gilí rakers are short and few in
dal fins are thin and deep. The dorsal fin extends well number. Balancers are absent. The dorsal and ventral
onto the body, and in young larvae the ventral fin may caudal fins are low and fleshy and extend the full length
bifúrcate around the vent and continué anteriorly onto of the tail. In many of these larvae the body is depressed.
the belly. This type of larva is characteristic of most Hy- This type of larva is characteristic of some Batrachuperus,
nobíus, Necturus, various salamandrids (Notophthalmus, Ranodon, Cryptobranchus, Proteus, Euproctus, Dicamp-
Pleurodeles, Tarícha, Trituras, and Ty/oíotritonJ, most todon, Rhyacosiredon, Ambysoma ordinaríum, and
Ambystoma, and some plethodontids (Hemidactylium, stream-dwelling plethodontids, such as Gyrinophilus,
Stereochilus, and Eurycea quadridigitata). All of these Pseudotriton, Typhlotriton, and most species of Des-
develop in ponds, but Tarícha riuu/aris does occur in mognathus and Eurycea.
quiet pools in streams. Neotenic salamanders of the fam- The mountain brook-type of larva has a guiar fold with
ily Sirenidae also have pond-type adaptations. no medial indentation (Fig. 6-10C). The gilí rami are
Stream-type larvae have a guiar fold that is only slightly short and bear a single row of small fimbriae; gilí rakers
indented midventrally (Fig. 6-10B). The gilí rami are long are absent or present only as small protrusions on the

Figure 6-12. Adaptive types of

tadpoles in quiet water. A. Rano
palmipes, a generalized grazer.
B. Megophrys montana, a surface
feeder. C. Ololygon nebulosa, which
lives amidst vegetation in midwater.
D. Gastrophryne carolinensis, a
midwater, microphagous type.
E. Hyla microcephala, a midwater,
macrophagous type. F. Qccidazyga
lima, a bottom-feeding type.

Figure 6-13. Mouths of tadpoles ínhabiting

ponds. A. Rana palmipes, a generalized grazer.
B. Megophrys montana, a surface feeder.
C. Hyla microcephala, a midwater,
macrophagous type. D. Ceratophrys cornuta, a
predaceous carnivore. See Figure 6-12 for body
shapes of A-C.
 Larvae
rami. Balancers are absent. Dorsal and ventral caudal fins 159
are low, fleshy, and present only on the distal half of the
tail. Examples of this type of larva include Onychodac-
ly/us, some Batmchuperus, and Rhyacotríton o/ympicus.

Anurans
The adaptive radiaüon among anuran larvae is far more
diverse than in salamanders. Orton (1953) defined se ven
adaptive types (including direct development) of tadpoles
based on posiüon and size of the mouth, shape of the
body, and development of the caudal musculature and
fins. These adaptive types should not be confused with
the basic morphological types of tadpoles presented ear-
Ber. Orton (1953) derived various adaptive types of tad-
poles from a generalized pond-type with an anteroventral
mouth and moderately developed caudal fins.
The generalized pond-type of tadpole is an aquatic
organism with a roughly ovoid body, a tail about twice
as long as the body with dorsal and ventral caudal fins
each about as deep as the caudal musculature, and an
anteroventrally directed mouth (Fig. 6-12A). The mouth
usually is bordered laterally and ventrally by one or two
rows of small papillae. The upper lip bears two or three
rows of keratinized denudes, and there are three or four
rows on the lower lip. The jaws bear keratinized beaks
with fine serrations (Fig. 6-13A). This is the pond-type of
tadpole common to many genera within the families Dis-
coglossidae, Pelobaüdae, Myobatrachidae, Leptodactyl-
idae, Bufonidae, Pseudidae, Hylidae, Ranidae, Hypero-
ttidae, and Rhacophoridae.
The adaptive radiation within pond-type tadpoles in-
volves modifications for life in different strata and feeding
on different-sized particles of food. Among the most strik-
ingly different adaptive types are the funnel-mouthed
surface feeders occurring in the genera Megophrys, Mi-
crohyla, and Phyllomedusa (Figs. 6-12B, 6-13B). These
tadpoles suspend from the surface tensión of forest ponds
Figure 6-14. Midwater filter-feeding types of tadpoles shown in
(quiet pools in streams in the case of Phyllomedusa) and characteristic planes of orientation. A. Xenopus laevis.
feed on various-sized particles of floating material. In such B. Rhinophrynus dorsalis. C. Agalychnis spurrelli. Denticles and
tadpoles, the broad mouth possibly provides not only a beaks are absent in Xenopus and Rhinophrynus; two upper and
three lower rows of denticles and horny beaks are present in
larger surface área for suspensión from the surface but a Agalychnis. Xenopus and Rhinophrynus have paired ventrolateral
larger food-gathering surface; denudes are greatly re- spiracles, and Agalychnis has a single spiracle just to the left of the
duced or absent. Some pond tadpoles have laterally midventral Une.
compressed bodies and very deep caudal fins, perhaps
best exemplified by some species of the hylid genus O/o/-
ygon (Fig. 6-12C). These tadpoles swim amidst dense pressed bodies, lateral spiracles, and elongate tails are
vegetation. The generalized pond-type and laterally com- bottom feeders or live amidst dense aquatic vegetation
pressed tadpoles graze on periphyton, leaves, and det- (Figs. 6-12E, 6-12F).
ritus. Nectonic filter-feeding tadpoles that characteristically
A variety of Hy/a and Occidozyga, among others, are feed in midwater have terminal mouths and thin caudal
macrophagous in ponds. Many of these tadpoles have fins that may be moderately low and long or shorter and
terminal mouths, lack denudes, and have either few large deeper. Nectonic tadpoles of Xenopus and Rhinophry-
or no labial papillae (Fig. 6-13C). Various shapes of bod- nus (Fig. 6-14) lack denticles and beaks and have elon-
ies and tails correspond to the strata in ponds where they gate barbéis at the border of the mouth. These tadpoles
feed; tadpoles with rounded bodies, ventral spiracles, and are oblígate filter-feeders, whereas the facultative filter-
normal caudal fins, such as those of many microhylids feeders of the hyperoliid Kassina and phyllomedusine
(Fig. 6-12D) live in midwater. Those tadpoles with de- hylids have denticles and beaks but no barbéis. Many,
LIFE HISTORY
160 '; . «
?• ;<.y-?:~*!«-...,,.
,s»,,»>>.•„.;.,'/•.; P

Figure 6-15. Adaptive types of

tadpoles in streams. A. Hyla
rivularis, a riffle inhabitant. B. Hyla
lindae, a riffle inhabitant.
C. Atelopus ignescens, with suctorial
disc for clinging to stones. D. Hyla
uranochroa, an inhabitant of pools.
E. Colostefhus nubicola, with
upturned terminal mouth for clinging
to lee sides of stones.
F. Centrolenella griffithsi, with an
elongate body and reduced fins for
living in litter or gravel.

and perhaps all, of these filter-feeders form conspecific tadpoles with no multiplication of rows of denudes, have
aggregations in midwater and have characterisüc orien- robust beaks with large serratíons.
taüons—level in Rhinophrynus, head down at about a Some stream-inhabitíng tadpoles are able to survive in
45° angle in pipids, and head up at about a 45° angle in torrentíal streams, but a clear distinction cannot be made
Kossina and phyllomedusine hylids. The tadpoles main- between stream and torrent tadpoles. Many of the tad-
tain their posiüons by constantly fluttering the üps of their poles that have large mouths and many rows of denudes
tails. not only use these buccal structures for scraping moss off
Tadpoles of many groups of frogs inhábil streams. Some rocks but also use their mouths for holding onto rocks
of these remain in quiet pools and exhibit no particular and thereby maintaining their positions in the strong cur-
morphological adaptaüons to life in flowing water, al- rent. However, some torrent-adapted tadpoles have de-
though some have proporüonately longer tails and shal- veloped a suctorial ventral disc with which they adhere
lower caudal fins than is characterisüc of tadpoles inhab- to rocks. Such a disc is present in the tadpoles of Asca-
iting ponds. Most stream-adapted tadpoles have ventral phus, the bufonids Ansonia and Atelopus, and the ranid
mouths, depressed bodies, long muscular tails, and shal- Amo/ops (Fig. 6-16C). Their suctorial discs are suffi-
low fleshy fins (Fig. 6-15). These tadpoles usually remain ciently effecüve that the tadpoles have to be pried off
on or near the substrate, and they characteristícally main- rocks; tadpoles of Atelopus even adhere to the under-
tain their position in the current by facing upstream and sides of rocks (Duellman and Lynch, 1969). The ventral
maintaining constant caudal movement. However, in quiet musculature is highly modified in the tadpoles of Amo-
pools they orient in various directions and may feed amidst lops (Noble, 1929a) and presumably so in the other gen-
accumulated leaf litter or other detritus. Most stream tad- era; furthermore, the lungs are small and develop late in
poles are grazers on algae growing on rocks in the streams. larval life. The mouths of these torrent-adapted tadpoles
These tadpoles have enlarged mouths, usually com- apparently function in the same way as those stream
pletely bordered by two or more rows of labial papillae, tadpoles that lack suctorial discs, except that the scraping
but in some stream tadpoles the median part of the upper action of the denudes takes place within the oral discs.
lip is bare. The number of rows of denudes is highly Tadpoles of Ascaphus rruei can extract food párteles from
variable; in some it is the same as in many pond tadpoles suspensión (Altig and Brodie, 1972), but, as noted by
(i.e., 2 upper and 3 lower rows), but the denudes are Gradwell (1973) and Wassersug (1980), there is no sup-
large and the rows long, extending to the labial papillae port for Noble's (1927b) suggesüon that these tadpoles
(Fig. 6-16). Some stream tadpoles have many rows of take in food through their nares.
denudes, as many as 9 upper and 14 lower rows in Hyla Some stream-inhabitíng tadpoles have funnel-shaped
claresignata (B. Lutz and Orton, 1946) and 4 upper and mouths (Fig. 6-16D). Tadpoles of this type (e.g., pelo-
17 lower rows in Heleophryne purcelli, which lacks beaks batids of the genus Leptobrachium and members of the
(Wager, 1965). The multiplication of rows of denudes in Hyla uranochroa and Ptychohyla schmidtorum groups)
a large mouth occurs in tadpoles of many families of inhabit relatívely quiet pools in streams and feed on loóse
anurans, including the pelobatids of the genus Scutiger, párteles of food. The reduction of the denudes suggests
the myobatrachid Megisío/oíis, the African Heleophryne, that they do not scrape moss or algae from rocks like
many hylids (some species of Hyla, Litaría, Nyctimystes, those stream tadpoles with large mouths and well-de-
and Ptychohyla), and many ranids (Conraua, Petrope- veloped denudes. The dendrobatíd Colostethus nubicola
detes, Tríchobatrachus, and some Asian Rana). Com- has a terminal funnel mouth (Fig. 6-15E) and feeds along
monly these tadpoles, as well as many stream-adapted the lee and undersides of rocks in streams. Tadpoles of
 Larvae
161
A

Figure 6-16. Mouths of tadpoles inhabiting

streams. A. Hyla rtvularís, with an enlarged
mouth but no increase in rows of denticles.
B. Hyla lindae, with an enlarged mouth and
an increased number of rows of denticles.
C. Atelopus ignescens, with a suctorial disc.
D. Hyla uranocftroa, with a ventral, funnel
mouth. See Figure 6-15 for body shapes.

Figure 6-17. Miscellaneous adaptive

types of tadpoles. A. Thoropa
petropolitana, semiterrestrial.
B. Leptopelis hyloides, terrestrial
to aquatic. C. Hyla bromeliacia,
an inhabitant of arbórea! bromeliads.
D. Anotheca ¡pinosa, oophagous.
E. Ceratophrys cantuta, carnivorous.
F. Stephopaedes anotis, with fleshy
crown surrounding eyes and nares.

centrolenid frogs have relatively small, unmodified mouths This same type of morphology is even more extreme
but greatly elongated bodies and tails with reduced, fleshy in the semiterrestrial larvae of some South American lep-
flns (Fig. 6-15F). Although they develop in fast-flowing todactylids. Tadpoles of Cyc/oramphus fuliginosas and
streams, these tadpoles generally do not live in open species of Thoropa wriggle though mud and creep over
water. Instead they are in the gravel or under rocks on wet rock faces (Wassersug and Heyer, 1983). In these
the bottom of the streams and thus are not subjected to tadpoles the flns are greatly reduced on the extremely
the rigors of flowing water. Their morphology seems to long, muscular tail; the body is elongated and depressed,
be an adaptaüon for movement within the gravelly sub- and the ventral part of the body may be flattened and
strate. expanded (Fig. 6-17A). The mouth is slightly enlarged,
LIFE HISTORY
162 anc j there is no proliferation of denudes. These tadpoles jaw and are concealed by a fleshy fold on the lower jaw
are very much like those of the closely related C. stejne- (Fig. 6-9). Each "dentícle" is composed of thin, hard
gerí, which have reduced mouthparts and complete their layers of cornified tissue; the outer layers apparently are
development with nutrients provided by the yolk (Heyer shed as the "denticle" grows.
and Crombie, 1979). The same feeding mechanisms are involved whether
Other kinds of tadpoles have long, muscular tails and the food eaten is phytoplankton, periphyton, small aquatic
reduced fins as adaptations for movement across wet organisms, or amphibian larvae. Thus, the hyobranchial
ground, in shallow cracks, or on leaves. Also the long pump mechanism opérales more or less contmuously in
tails may be important as respiratory structures. Tadpoles nektonic Xenopus tadpoles, but it is this same pumping
of the hyperoliid genus Leptopelis have relatively long mechanism that is used in the ingestión of small aquatic
tails and reduced fins (Fig. 6-17B); these tadpoles wriggle invertebrates by Hymenochirus (Sokol, 1962, 1969).
from a terrestrial nest to ponds (Oldham, 1977). Tad- Oophagous tadpoles apparently ingest enüre anuran eggs,
poles of Leptodactylus rugosus also have long, muscular but the mechanism of ingestión is not known. Two gen-
tails with reduced fins; these slender tadpoles live in shal- era of African bufonids have tadpoles that differ from all
low cracks on granitíc rock and can move from one water- others by having a thick crown surrounding the eyes and
filled crack to another by violently flipping the tail and nostrils, with the mouth opening just below the ventral
thus propelling themselves across rock. Some tadpoles edge of the crown (Fig. 6-17F). The tadpoles of Stepho-
that live in bromeliads, such as Osteopilus brunneus and paedes anotis were observed in a stagnant pool between
Hyla maríanae in Jamaica (E. Dunn, 1926a) and H. bro- tree buttresses; the crown was in contact with the air
meliacia and H. dendroscarta in Middle America (Duell- while the tadpoles clung to the bark in a tail-down po-
man, 1970) also have elongate bodies and muscular tails sition (Channing, 1978). The crown, composed of spongy
with low fins (Fig. 6-17C). These tadpoles move about connective tissue, may be an accessory respiratory sur-^
on the wet leaves of arbórea! bromeliads. face or may function to keep surface scum away from
Various tadpoles that develop in bromeliads or tree- the nostrils (Channing, 1978). In Mertensophryne mi-
holes eat anuran eggs. Oophagous habits are known for cranotis the crown is used to suspend the tadpole at the
some Jamaican and Central American Hyla (E. Dunn, surface (Grandison and Ashe, 1983).
. 1926a, 1937), Anotheca (E. Taylor, 1954), some species The recent discoveries of peculiar modifications of some
of Dendrobates (Weygoldt, 1980; H. Zimmerman and E. African bufonids and the tadpole of Otophryne robusta
Zimmerman, 1981), Philautus (Wassersug et al., 1981), reveal that there still is much to be learned about the
and Hoplophryne (Noble, 1929a). The mouths of these structural modifications and their functional significance
tadpoles are terminal or subterminal and have large beaks in tadpoles.
but few or no denticles (Fig. 6-17D).
Many kinds of tadpoles are facultatively carnivorous
and are cannibalistic under crowded conditions or with PHYSIOLOGY AND ECOLOGY
a limited food supply. Tadpoles of Dendrobates auratus Amphibian larvae develop in a great variety of aquatic
developing in a water-filled cavity in a log have been habitats. Some occur in environmentally stable habitáis
observed to grow at different rates, with the larger indi- having nearly constant temperature and oxygen concen-
viduáis eventually eating their smaller siblings. Carnivory, trations, whereas others develop in environmentally less
especially cannibalism, is common among tadpoles that stable aquatic situations that are sqbject to considerable
develop in temporary ponds in and regions; this has been variations in temperature and therefore oxygen concen-
noted especially for Rhinophrynus, Scaphiopus, Lepi- trations. Some of these environmental variables affect
dobatrachus, and Puxicep/w/us. Lechriodus not only feeds respiratory and growth rates and provide constraints on
on tadpoles but carcasses of dead frogs (A. Martín, 1968). the adaptive types of larvae that can develop successfully
The tadpoles of Leptodactylus pentadactylus are noto- in different aquatic habitats. Moreover, some combina-
rious predators on other kinds of tadpoles (Heyer et al., tions of these environmental variables may influence the
1975; Kluge, 1981). However, most of these tadpoles behavior of the larvae. Population dynamics of larvae are
do not exhibit any specific adaptations for carnivory like treated in Chapters 2 and 11, and interspecific interac-
those of Ceratophrys that have anterior mouths, rela- tions are discussed in Chapter 12.
tively massive jaw musculature, and large," strongly ser-
rated beaks (Figs. 6-13D, 6-17E). Phototaxis
The presumably predaceous tadpole of the microhylid Although most adult amphibians are negatively photo-
Otophryne robusta, which develops in sand bars in tactic, larvae exhibit a variety of responses to light. Gen-
streams, is unique among known tadpoles in having a erally salamander larvae in ponds and anuran larvae in
long, sinistral spiracular tube that extends posteriorly to streams are negatively phototactic, whereas the opposite
the midlength of the tail and a single row of long, pointed is true in salamander larvae in streams and anuran larvae
denticle-like structures on the margin of each jaw (Py- in ponds. However, there are exceptions and even on-
burn, 1980b). Beaks and normal labial denticles are ab- togenetic shifts in phototactic responses.
sent, and the sharp "denticles" protrude from the upper Observations on activity cycles of Ambystoma reveal
 Larvae
fíat larvae developing in ponds at low elevations, where absorption by visual pigments (Liebman and Entine, 1968), 163
Kmperatures are relaüvely warm, are negatively photo- and this could account for the ontogenetic changes in
Bctic (J. Anderson and Graham, 1967; J. Anderson and phototactic responses.
WilBamson, 1974; Marangio, 1975). However, larvae Investigations on compass orientation in larval am-
developing in montane streams or lakes, where temper- phibians have shown that there is a Y-axis orientation.
antes are comparatively cooler, are positively phototacüc Celestial orientation in tadpoles of Bu/o uioodhousii, .Rana
II Anderson and Worthington, 1971; J. Anderson, 1972). catesbeiana, R. c/amitans, and Gastrophryne cara/inensis
A notable exception is A. maculatum, which is positively is away from the shoreline toward deeper water until
phototactic in warm ponds (C. Schneider, 1968). Abrupt metamorphosis, when orientation shifts 180° toward land
dianges in light intensity have the most noticeable effect (Goodyear and Altig, 1971; Justis and D. Taylor, 1976).
in phototactic response of A. opacum; normally larvae Larvae of Ambystoma maculatum, opacum, talpoideum
ságrate into open water of ponds on dark nights. This is and tigrinum use solar cues in Y-axis orientation and also
especially so on dark nights following bright, sunny days; have the same 180° shift in orientation at metamorphosis
Ifocre is less noticeable activity on cloudy days or moonlit (Tomson and Ferguson, 1972; D. Taylor, 1972). Larvae
«ghts, but a total eclipse of the moon resulted in rapid ofA. tigrinum and R. catesbeiana can perceive solar cues
•¿gration of larvae to open water (Hassinger and J. An- extraocularly for sun-compass orientation and for syn-
derson, 1970). Nocturnal activity by Ambystoma larvae chronization of their biological docks; experimental re-
does not result in distinct stratification of larvae in the sults suggest that the pineal body and/or frontal organ
water column (L. Branch and Alttg, 1981). The floating are involved in extraocular photoreception (D. Taylor,
behavior by A. tigrinum larvae is dependent on buoy- 1972; Justis and D. Taylor, 1976).
ancy; air breathing and availability of pelagic prey are Some of the observed phototactic behaviors of am-
correlated with floating (Lannoo and M. Bachmann, phibian larvae may be partial responses to temperature
1984b). gradients. Vertical migration and interspecific stratification
Positíve phototaxis has been demonstrated or ob- in ponds at night by Ambystoma larvae may be initiated
served in tadpoles of many species of the genera Bu/o, by darkness with subsequent stratification dependent on
Hyla, and Rana, plus Xenopus íaeuis and Aga/ychnis cal- different preferred temperaturas. Because the larvae are
Idryas inhabiting warm ponds (Ashby, 1969; Duellman, feeding in open water at night, their vertical migration
1970; R. Jaeger and Hailman, 1976; Beiswenger, 1977). and stratification also could be influenced by the spatial
Likewise, tadpoles of B. canorus and R. pretiosa inhab- distribution of prey in the water column (J. Anderson and
ijng cold montane ponds are positively phototactic (Mul- Graham, 1967). In pond-dwelling tadpoles, response to
Wy, 1953; L. Licht, 1975). Also, Duellman and Trueb increasing light intensity rather than to more slowly in-
have observed positive phototaxis in tadpoles of B. spi- creasing temperature would give larvae additional time
nulosus, Pleurodema marmorata, Gastrotheca marsu- in the morning for feeding and moving into optimal áreas;
piata, and G. riobambae in cold ponds at high elevations positive phototaxis also allows the tadpoles to anticípate
án the Andes. heating of shallow áreas and to move into them just as
Tadpoles inhabiting cool montane streams seem to be they are beginning to warm, thus providing máximum
negatively phototactic; this conclusión is based on the use of the heat for metabolism and growth. Therefore,
observaüons of Ascaphus truei by deVlaming and Bury tadpoles aggregating in warm shallow water may have
11970) and Duellman and Trueb's extensive observa- responded initially to light (Beiswenger, 1977). Likewise,
fions on many species of Hyla, Plectrohyh, Ptychohy/a, negative phototaxis among stream-inhabiting tadpoles may
and Telmatobius. If tadpoles of these species are active be importan! in the avoidance of pools in which tem-
at all by day, they tend to be in shaded áreas of the peratures exceed their thermal preferences.
streams. Pools in streams that seem to be devoid of tad- However, not all phototactic responses may be so sim-
poles by day may contain many individuáis at night. ple. The Y-axis orientation away from shore seems to
Limited data are available on ontogenetic changes in contradict the general observations of the influences of
phototaxis during the larval stages. Larvae of Ambystoma light and temperature on aggregation in warm shallow
opacum are positively phototactic until their hindlimbs water. Therefore, this orientation may be more closely
are fully developed; subsequently they are negatively associated with escape behavior, for when tadpoles in
phototactic (Marangio, 1975). Young larval Eurycea bis- shallow water are disturbed they invariably flee away from
íneata are less sensitivo to light than older larvae (J. Wood, shore. The green spectral preference of tadpoles without
1951). Ontogenetic spectral shifts in phototaxis have been hindlimbs can be associated with green plants (Muntz,
demonstrated in Xenopus laevis, Bufo americanus, ñaña 1963b); perhaps color visión, along with olfaction, is im-
pipiens, and R. temporaria (Muntz, 1963b; R. Jaeger and portant in locating food (R. Jaeger and Hailman, 1976).
Hailman, 1976). At early stages the response was strongly
toward green light; at midstages response to blue and Thermal Preferences and Tolerances
green were nearly equal, but preference for blue pre- It is well known that aquatic ectotherms adopt various
dominated after the eruption of the forelimbs. There is behavioral, biochemical, and physiological strategies to
an ontogenetic spectral shift to shorter wavelengths in minimize the effects of varying ambient temperature on
LIFE HISTORY
164 their metabolic processes. The difficulty in assessing the ians that live in cooler environments usually have notably
temperature responsos of amphibian larvae in nature and lower tolerances to heat. The highest temperatures to-
the variation in experimental design of laboratory studies lerated (LD50) by Rana sy/uafica in Alaska is 36°C (Her-
lead to difficulty in ascertaining the effects of temperature reid and Kinney, 1967), and larvae of newts, Taricha
on the larvae in nature. Consequently, different studies riuu/aris, tolérate temperatures of only 34°C (P. Licht and
have provided conflicting results. Metabolic compensa- A. Brown, 1967).
üon may be determined from a rate-temperature curve Different species living under the same climatíc regime
of temperature-dependent rate functions; in ectotherms exhibit differences in tolerances to rates of heating. In
this curve may be modified by the organism's previous Puerto Rico, tadpoles of Leptodacty/us a/bi/abris heated
thermal experience. at a rate of l°C/minute died at temperatures of 39.5 to
Thermal preferences in larvae of Ambystoma tigrinum, 41.0°C, whereas those heated at l°C/5 minute survived
Rana catesbeiana, and R. pipiens are dependent on their unül temperatures of 40 to 42°C; tadpoles of Bu/o mar-
previous acclimation (Lucas and Reynolds, 1960). Heat inus heated at the two rates all died at 44 to 45.6°C
resistance in tadpoles of Scaphiopus couchü, S. ham- (Heatwole et al., 1968).
mondii, Hy/a regi//a, and Osteopi/us septentriona/is can However, in nature and in laboratory experiments pro-
be increased by warm thermal histories (H. Brown, 1969). viding a thermal gradient, larvae demónstrate preferred
These observations suggest compensatory abilities. How- temperatures. These range from 9 to 29°C in Rana syí-
ever, experiments on tadpoles of R. pipiens (G. Parker, uatica with a mode of 19 to 20°C (Herreid and Kinney,
1967) and Limnodynostesperoni (B. Marshall and Grigg, 1967), whereas the mode is 30°C in Bu/o terrestris (No-
1980) showed an absence of ability to acclimate meta- land and Ultsch, 1981), but only 23 to 24°C in Taricha
bolically. riuu/aris (P. Licht and A. Brown, 1967) and 25°C in Am-
Most experiments with temperature adaptaüons of am- bystoma tigrinum (Lucas and Reynolds, 1960).
phibian larvae have emphasized critical thermal máxima In most studies in which developmental stage has been
with respect to thermal acclimation. Larvae acclimated at associated with temperature, the results show that younger
higher temperatures have greater heat resistance and larvae have greater heat resistance and broader ranges
therefore higher thermal máxima than larvae acclimated of tolerance than older larvae. However, first-year tad-
to lower temperatures (Fig. 6-18). The tadpoles of most poles of Ascaphus truei prefer temperatures below 10°C,
anurans succumb at temperatures of 38 to 40°C, but whereas second-year tadpoles prefer temperatures of 10
some species that develop in shallow ponds in xeric or to 22°C (deVlaming and Bury, 1970).
tropical regions tolérate higher temperatures—above 41°C Intraspecific geographic and altítudinal differences in
in Scaphiopus couchii and Osteopi/us septentriona/is heat tolerances are known for a few larvae. Montane
(H. Brown, 1969), 39.2°C in Cyc/orana cu/tripes, C. p/a- larvae of Ambystoma tigrinum acclimated at 20°C toler-
íycepha/a, and Litoria rubeí/a (Main, 1968), 40.4°C in ated significantly higher critical máximum temperatures
Leptodacty/us a/bi/abris (Heatwole et al, 1968), 42°C in than larvae from low deserts, but larvae from both sites
Rana cancriuora (Dunson, 1977), and 41.8°C in Bu/o acclimated at 10°C showed no significant differences
terrestris (Noland and Ultsch, 1981). However, amphib- (Delson and Whitford, 1973). This is the opposite of the
gradient observed in Pseudacris triseriaía, in which tad-
poles from lower elevaüons had higher critical thermal
máxima than those from the high mountains (Hoppe,
42 1978). On the other hand, no significant differences were
found in heat resistance between lowland and highland
^40 tadpoles of Leptodacty/us a/bi/abris (Heatwole et al., 1968).
S? Studies on the role of temperature adaptaüon in the
D
ecology and distributíon of amphibians generally support
Ushakov's (1964) contenüon that differences in temper-
ature tolerances are importan! in speciation. This idea is
I supported further by the intermedíate temperature tol-
15 36 erances of hybrids between parental species Scaphiopus
x:
hammondii and S. mu/tip/icatus (H. Brown, 1969).
34
Respiration
10 15 20 25 30 35 Respiraüon by amphibian larvae may be branchial, cu-
Acclimation Temperature (°C) taneous, and/or pulmonary. Thorough studies have in-
volved only a few species of Ambystoma, Xenopus, Bu/o,
Figure 6-18. Relationships between incipient lethal temperature and Rana. From the results of these limited investigations,
(LD50) and acclimation temperature in tadpoles. A. Scaphiopus
couchii. B. Osteopifus septentriona/is. C. Scaphiopus hammondii. some generalities seem to be apparent, but applicaüon
D. Hyla regula. Adapted from H. Brown (1969). of them to the broad spectrum of amphibian larvae must
 Larvae
be done with cautíon and necessarily should include careful do not develop untíl just before metamorphosis in stream- 165
comparative studies. adapted larvae and in Bu/o; thus, these tadpoles cannot
Among salamander larvae, at high oxygen concentra- effectively consume oxygen by gulping air. Gulping air is
tions the gills perform only a small part of the total res- unnecessary by tadpoles in well-oxygenated streams; fur-
piration; the majority is cutaneous. At low oxygen con- thermore, air bubbles would increase their buoyancy,
centrations, larvae of Ambystoma maculatum that have which would be detrimental to hydrodynamics. At low
had their gills removed have lower respiratory rates than concentrations of oxygen, Bu/o tadpoles swim at the sur-
larvae with gills (Boell et al., 1963). Experiments on un- face of the water; at such times these tadpoles may sup-
altered larvae of the same species show that during their plement branchial respiration with cutaneous respiration.
development larvae become progressively less tolerant The relationships among oxygen contení, body size,
of low oxygen concentrations (L. Branch and D. Taylor, respiratory behavior, and locomotor stamina in tadpoles
1977). In experiments by Bond (1960), the fimbrial área of Xenopus laevis, Bufo amerícanus, and Rana berían-
of gills oíA. jeffersonianum, A. opacum, and Salamandra dierí were investigated by Peder (1983a), who demon-
salamandra increase in size in response to lowered oxy- strated that respiratory patterns may have major effects
gen concentrations. These changes involve an increase on locomotor capacities and that locomotion may alter
in number and size of cells in the fimbrae; however, the respiratory patterns. The problems of gas exchange are
changes are reversible, depending on the oxygen con- associated with those of hydrodynamics and locomotion
centraüon. The mudpuppy, Necturus maculosus, relies in the following ways: (1) locomotor activity increases the
largely on cutaneous respiraüon at low temperatures, but demand for oxygen either during activity, after activity
at higher temperatures (and therefore lower oxygen con- ceases (oxygen debt), or both; (2) aerial and aquatic res-
centrations) or when the salamanders are disturbed, the piratory surfaces are importan! in meeting this increased
gills assume the dominant role in respiraüon (Guimond oxygen demand; (3) irrigation of aquatic respiratory sur-
and V. Hutchinson, 1972). Likewise, at 25°C larval faces (gills) is in part counterproductive because it in-
A. tigrinum take in about 59% of their total oxygen from creases drag and therefore locomotor effort; (4) ventila-
the water; the rest is acquired via the lungs by gulping tion of aerial respiratory surfaces (gulping air) is in part
air (Whitford and R. Sherman, 1968). counterproductive because it increases buoyancy and
Respiratory rates for larval anurans were summarized promotes hydrodynamic instability (at least in flowing
by Peder (1981), who demonstrated that body size, trophic water); and (5) any increase in respiratory activity may
state, diel cycles, and experimental stress all influenced increase the demand for oxygen.
rates of oxygen consumption by tadpoles of Xenopus Tadpoles of some species are capable of existing out
¡aevis and Rana bertandierí; he concluded that the results of water in moist terrestrial environments, but respiratory
of much of the earlier work on metabolic rates of tadpoles rates of such tadpoles have not been studied. Tadpoles
must be viewed with caution because mpst investigators of Leptodactylus albilabrís hatch from eggs laid in terres-
had not recognized the effects of these variables. Exper- trial chambers that subsequently are flooded. These tad-
iments with larvae of Hymenochims boettgeri, X. laevis, poles have been maintained on moist cortón in the labo-
Bufo woodhousü, andR beríandierí (Peder, 1981, 1982c) ratory for up to 40 days; under these conditions the
have shown that at a constant temperature body size respiratory rates declined greatly but retumed to normal
accounts for most of the variance in rates of oxygen con- when the tadpoles were replaced in water (Candelas et
sumption in these tadpoles and that reported differences al., 1961).
in rates at different developmental stages are related to
size. There is an increased rate of oxygen consumption Salt Balance
with increased size; however, in late developmental stages Most amphibian larvae are intolerant of saline conditions,
of some X. laevis, oxygen consumption decreases, pre- and their nitrogenous wastes are almost exclusively am-
sumably because of their reduced physical acüvity. Rates monia, which is readily diluted in water. However, there
of oxygen consumption increase with higher tempera- are exceptions to both of these generalities.
tures in tadpoles of R. pipiens (G. Parker, 1967) and In Sweden, Bu/o virtáis frequently breeds in brackish
Limnodynosíes peroni (B. Marshall and Grigg, 1980). water, and tadpoles survive in water that is 15% of the
Amphibian larvae with lungs respond to low concen- salí concentration of sea water (Gislén and Kauri, 1959).
trations of oxygen by increasing the rate of pulmonary Rana cancriuora is a common inhabitant of brackish
ventüaüon (Wassersug and Seibert, 1975). They also may mangrove swamps in southeastern Asia, and its tadpoles
increase the rates of branchial irrigation (N. West and are capable of development in brackish water. Experi-
Burggren, 1982) and anaerobic metabolism (Weigmann ments by Dunson (1977) showed 100% survival of tad-
and Alüg, 1975). poles in concentrations up to 40% sea water and more
As the amount of dissolved oxygen decreases, most than 50% survival in concentrations of 80% sea water.
iadpoles can consume more oxygen by gulping air. This The tadpoles of some species of leptodactylids that
behavior is especially conspicuous in pond-inhabiting develop in foam nests have high tolerances to urea. Tad-
tadpoles that develop lungs early in their larval life. Lungs poles of Leptodactylus albilabrís (Candelas and Gómez,
LIFE HISTORY
166 1963) and L. bu/onius (Shoemaker and McClanahan, selection may be importan! in the selectíon of prey types.
1973) initiate a high level of urea production as embryos Henderson (1973) showed that larval A. graci/e selected
(see Chapter 5); throughout their larval development they particular microhabitats through increased encounter rates
have rates of nitrogen excretion essentially equivalen! to of prey types in association with a particular microhabitat.
those of other kinds of tadpoles, but in these species of Larvae of many kinds of salamanders are known to
Leptodacty/us the level of ammonia excretion remains prey on smaller amphibian larvae, especially under labo-
nearly constant while the rate of urea excretion increases ratory conditions when the food supply is inadequate,
with age, only to decline at metamorphosis. Possibly the but there also are documented cases of this behavior in
ratío of urea to ammonia is determined by the total rate nature. The large larvae of Dicamptodon ensatas are
of nitrogen excretion, but the percentage of total nitrogen especially predatory. At one site, tadpoles of Ascaphus
excreted as ammonia also may be related to the avail- truel formed 14% of the diet (Metter, 1963), and at an-
ability of water. other site 39% of the stomach contents were larvae of
Ambysíoma graci/e (C. Johnson and Schreck, 1969).
Feeding Larvae of Ambystoma tigrinum feed on larvae of Rana
Most salamander larvae feed indiscriminately on aquatic sy/uatica and other species of Ambystoma (Wilbur, 1972).
invertebrates of appropriate sizes. However, some larval Larvae of Tn'turus alpestris prey on tadpoles of several
newts (Notophthatmus and Trituras) feed on algae (C. sympatric anurans—Bombina uariegata, Rana ridibunda,
Pope, 1924; Creed, 1964). In some populations of Am- and R. temporaria, but not on Bu/o calamita (Heusser,
bystoma tigrinum, larvae have a coiled gut, perhaps in- 1971). In alpine ponds, larger larvae of Salamandra sal-
dicative of herbivory (Tilley, 1964). The limited evidence amandra feed on smaller conspecifics (Parátre, 1894);
on ontogenetic changes in food and foraging strategies the same occurs in Typh/otriton speleaus in subterranean
of salamander larvae suggests that these differences are waters (C. C. Smith, 1959). Cannibalism in these pop-
partly associated with gape-limited predation. Young lar- ulations may be the result of low incidence of other kinds
val A. macrodacty/um are rather sedentary and simply of food.
snap at prey passing by, whereas older larvae are much In some populations of Ambystoma tigrinum three lar-
more agüe and stalk prey (J. Anderson, 1967). Likewise, val and adult morphs are found. A large morph inhabits
young larval A. opacum feed on the bottom of ponds, permanent ponds and commonly does not metamor-
whereas larger larvae actively forage in the water column phose; a small morph inhabits ephemeral ponds and
(J. Anderson and Graham, 1967; Marangio, 1975). A metamorphoses. The larvae of these two morphs are
similar ontogenetic shift in feeding behavior occurs in normal in their morphology and feeding habits for pond-
larvae of Tn'turus vulgaris, for which G. Bell (1975) sug- dwelling Ambystoma. Cannibal morphs are like the small
gested that an exponential rate of weight gain forces larger morphs in habitat and life history, but they have dispro-
larvae to switch from passive to active foraging, thus en- portionately large heads, wide mouths, and elongate teeth
abling them to catch larger prey but at the expense of (Fig. 6-19), and they prey on conspecific larvae (F. Rose
incurring a higher rate of mortality. In the stream-dwelling and Armentrout, 1976). Slight differences in allozyme
Leurognathus marmoratus, diets of larvae are composed frequencies exist between cannibals and noncannibals,
of nearly the same diversity of insects as the aquatic adults, but these are less than the magnitude of differences be-
except that the adults eat larger prey (Martof and D. tween subspecies of A. tigrinum (Pierce et al., 1981).
Scott, 1957). On the other hand, learned microhabitat Experiments by Collins and Cheek (1983) suggest that

Figure 6-19. Normal and

cannibalistic morphs of Ambystoma
tigrinum. Upper row—larval and
adult normal morph. Lower row—
larval and adult cannibalistic morph.
Adapted from F. Rose and
Armentrout (1976).
 Larvae
hnal density stimulated expression of cannibalistic traits. tadpoles are included in the foregoing sectíon: Adaptive 167
¡ adaptive significance of the cannibalistic morphs in- Types of Larvae. In addiüon to the oophagous species
not only greater prey availability because of in- discussed there, other species have been observed to
oeased gape but also more rapid growth and therefore ingest amphibian eggs. This facultative habit is known for
metamorphosis (Lannoo and M. Bachmann, tadpoles of Rana temporaria, which eat conspecific eggs,
|JB84a). as well as those of six other anurans (Heusser, 1970a).
k contrast to the larvae of salamanders, anuran larvae A tadpole of Leptodactylus labyrinthicus ate eggs of Hyla
mu primarily highly specialized fllter-feeders. Tadpoles albopunctata (Cardóse and Sazima, 1977).
i a mechanism for extracüng suspended particles of
I from water (Kenny, 1969b, Severtzov, 1969; Was-
1972). The following synthesis of feeding is sum- Growth
¡«•rized from Wassersug (1980). Growth rates are dependent primarily on temperature
Most of the internal oral structures of tadpoles make and food availability. Most pond-dwelling larvae have a
p a multitiered, parücle-entrapping system that is ca- sigmoidal growth curve, whereas the rate in stream-
Bbie of sorting particles by size. Direct interception and dwelling salamander larvae is more nearly curvilinear.
¡ÜBrtial impaction are used to different extents on various There is a positive correlation between growth rate and
«races. The mucous surfaces of the branchial food traps, ovum size in Ambystoma maculatum (DuShane and
fcgether with the gilí filters of the pharynx, can trap the C. Hutchinson, 1944). Growth studies of Ambystoma
particles ingested by typical pond larvae. Large summarized by Salthe and Mecham (1974) show that
i fHtiicles are strained from the water by buccal papillae larvae of A. tigrinum grow faster than those of A. ma-
í m¿ funneled directly into the esophagus, thereby by- cu/atum and that larvae of A. mexicanum grow faster
¡ passng most of the pharynx. This size-sorting mechanism than those of A. opacum. Also, growth rates in a cohort
; potects the delicate pharyngeal surfaces from clogging of A. tigrinum were found to be more variable than the
m damage by large particles. rates in a cohort of A. maculatum (C. Hutchinson and
From the size, shape, number, and arrangement of Hewitt, 1935). Higher respiratory rates of A. tigrinum
toccal and pharyngeal structures, it is possible to infer larvae, as compared with A. maculatum (Hopkins and
the size of the particles on which a species feeds most Handford, 1943), correlate with the differences in growth
tiently. Intraspecific differences in these structures pre- rates in these two species.
ably reflect differences in size distribution of food par- Growth rates within cohorts of anuran larvae are known
fcies in the microhabitats of the tadpoles. Compared with to be highly variable. This variaüon has been attributed
§eneralized tadpoles, in extreme macrophagous larvae to the availability of food and to a growth inhibition sub-
(eg.. Hyla leucophyllata and H. microcephala groups stance. However, Travis (1983) showed that in Hyla gra-
arad Occidozyga) all pharyngeal structures associated with tiosa the duraüon of the larval period was inversely re-
pfenktonic entrapment are reduced. Larvae that are ob- lated to early larval growth and that this relationship
fc£tte microphagous suspensión feeders in midwater (e.g., appeared to be strengthened slightly at increased densi-
Xenopus and many phyllomedusine hylids) have the op- ties. Observations and experiments on tadpoles of Eu-
posite extreme; they have large branchial baskets and ropean species of Rana and Bufo (R. Savage, 1952)
dense gilí filters that effectively entrap small phytoplank- showed that larger, more aggressive larvae outcompeted
*JTL Stream-inhabiting tadpoles are benthic and thig- smaller siblings for food. Similar results were obtained ¡n
motactic (e.g., Ansonia, Atelopus, and Plectrohyla). By studies of B. americanus and R. sylvatica (Wilbur, 1977b,
soaping pieriphyton with their keraünized mouthparts, they 1977c).
créate a coarse suspensión of párteles; they have closely A "crowding effect" resulting in inhibition of growth of
spaced, supemumerary buccal papillae for straining coarse smaller tadpoles by a chemical substance was observed
particles but highly porous gilí filters not suited for the in Rana pipiens larvae (C. Richards, 1958; S. Rose, 1960;
entrapment of ultraplankton. Umbrella-mouthed tad- L. West, 1960). The growth rate of small tadpoles is
poles (e.g., Megophrys and some Microhyla) feed selec- inhibited when they are raised in water in which larger
lh«ly on large particles floatíng on the surface of the tadpoles have lived. The growth-inhibiüng substance is a
water; instead of buccal papillae, they have ridges that proteinaceous compound produced by larger tadpoles
sort coarse particles. (Runkova et al., 1974; Stepanova, 1974). Most labora-
Developmental differences among siblings of Scaphio- tory experiments have dealt with intraspecific inhibition
pus bombifrons result in some individuáis developing effects, but growth rates of young tadpoles of Bufo cal-
normally as scraping suspensión feeders and others de- amita are inhibited when the tadpoles are raised in water
weloping larger and more serrate beaks, enlarged jaw conditioned by large tadpoles of R. temporaria and B.
muscles, and modificaüons of the denudes (Orion, 1954; bufo, and especially by older conspecifics (Heusser,
Bragg, 1965). The latter are highly predaceous on tad- 1972a). Moreover, different inhibitory effects were noted
poles of other species of Scaphiopus and are even can- for the different members of the Rana esculenta complex
nibalistic. (Heusser and Blankenhorn, 1973). Intra- and interspe-
Further details about feeding and foraging strategies in cific effects also were found with Bufo woodhousü (L.
LIFE HISTORY
168 Licht, 1967) and R. temporaria (Heusser, 1972b). Inhi- rican R. fuscigula may spend 3 years in ponds before
bition seems to occur in some natural populations of metamorphosing (Wager, 1965).
R. temporaria (Pikulik, 1977). However, laboratory ex- The duration of larval development in salamanders
periments on that species (Hodler, 1958) and on R. pi- varíes from 42 days in HemidactyKum scutatum to 5 years
pierts (Gromko et al., 1973), in which the tadpoles were in Cryptobranchus alleganiensis and Necturus maculosus
always provided with an excess of food, showed no growth (Bishop, 1941). Larvae of most ambystomatids and sal-
inhibition. Experiments on the tadpoles of Scaphiopus amandrids that develop in ponds require 2 to 5 months
holbrootó by Semlitsch and Caldwell (1982) revealed dif- from hatching to metamorphosis, but developmental times
ferentíal growth rates at high densities. Those tadpoles are longer for species developing in streams—3.5 years
reared at high densities that gained an early growth ad- in Rhyacotriton o/ympicus (Nussbaum and Tait, 1977)
vantage presumably metamorphosed at the minimum size and Gyrinophi/us porphyriticus (Bishop, 1941), 2 to 3
possible so as to escape the density stress. This relieved years in Eurycea bislineata (Duellman and J. Wood, 1954),
density stress on smaller tadpoles, which then increased 2 years in Desmognathus quadramaculatus, and 1 year
their growth rates and size at metamorphosis. These re- inD. fuscas, montícola, and ochrophaeus (Organ, 1961).
sults support Steinwascher's (1978) contenüon that larger Larvae of some Ambystoma that breed in the spring
tadpoles of R. sphenocephala outcompete smaller ones overwinter; this is an excepüon in A. maculatum in Mary-
for food (exploitative competitíon) and that as the relative land (Hillis and R. Miller, 1976) and elsewhere, but it is
level of food decreases, chemical inhibition (interference common in montane populations of A. macrodactylum
competition) supplants exploitative competition. Stein- (J. Anderson, 1967), A. gracile (Eagleson, 1976), and
wascher suggested that in nature, exploitative and inter- A. íigrinum (Bizer, 1978).
ference mechanisms could be complementary, and a switch With the excepüon of food availability, temperature
to interference mechanisms at low food levéis might be seems to be the major externa! factor controlling the
common. This suggestion needs to be tested both intra- duration of development and differentiation. Larval de-
and interspecifically. velopment in Rana catesbeiana ceases at temperaturas
The duration of larval development vanes from about of 12.8°C or lower (Viparina and Just, 1975). Low tem-
2 weeks in some anurans to as long as 5 years in some peratures halt metamorphic processes by depressing
salamanders. The most rapid development occurs in neuroendocrine and thyroid activity (Voitkevich, 1963),
anuran larvae developing in temporary ponds in arid en- thereby preventing a rise in circulating thyroid hormones
vironments. North American spadefoots, Scaphiopus, are occurring in natural metamorphosis (Just, 1972) and pro-
among the most rapidly developing tadpoles—S. bom- hibiting tissue responsos to existing circulating hormones
bi/rons 13-15 days (King, 1960; Voss, 1961), S. couchii (Ashley et al., 1968).
and S. holbroofá 14-15 days (A. H. Wright and A. A. Another facet of larval development is the amount of
Wright, 1949). The South African ranids Cacostemum yolk reserve when the larvae hatch. Of course, some
nanum and Pyxícepha/us adspereus may metamorphose larvae have a sufficient amount of yolk to reach meta-
in 15 and 18 days after hatching, respecüvely (Wager, morphosis (see Chapter 2 for examples). Others are pro-
1965). The Australian myobatrachid Notaden nichollsi vided with a small amount of yolk that is utilized before
may spend as few as 14 days as a tadpole (Slater and the larvae begin to feed. For example, larvae of Pseu-
Main, 1963). Although most tropical species of anurans dotriton ruber spend 6 to 10 weeks in streams before
require 3 weeks to 2 months, and températe species 2 they begin to feed (R. Cordón, 1966). Back-riding tad-
to 3 months, there are some notable exceptíons. The poles of Co/ostethus inguinalis have a small yolk reserve
North American Hyh avivoca requires only 24 days (Volpe and grow slightly while adhering to the mother's back
et al., 1961). (Wells, 1980c).
Tadpoles of some species of Rana in North America In general, larvae that reach a large size have a longer
and Eurasia overwinter in ponds—R. catesbeiana (Vi- larval period than those that metamorphose at a smaller
parina and Just, 1975), R. pretiosa (F. Turner, 1958), size, but there are numerous exceptions. The aquatic South
R. rugosa (Okada, 1966), R. septentrional® (Hedeen, American frog Pseudis paradoxa is renowned for its giant
1971). Tadpoles of R. clamitans developing in temporary tadpole, which on Trinidad attains a length of 230 mm,
ponds metamorphose during their first summer, whereas whereas adult female frogs are no more than 73 mm
those in permanent water may overwinter (Richmond, long; the tadpoles reach their full size in 4 months (Kenny,
1964). Tadpoles of the large leptodactylid Caudiverbera 1969a). A great size discrepancy exists between adults
caudiverbera in austral South America commonly require and tadpoles of the South African hyperoliid Kossina ma-
2 years to metamorphose (Cei, 1962). Tadpoles that de- cu/ata; tadpoles require 8 to 10 months to attain lengths
velop in cold mountain streams also have long larval of about 130 mm before metamorphosing into frogs that
development—3 years in Ascaphus truei (Noble and P. attain lengths of about 60 mm (Wager, 1965).
Putnam, 1931), 2 years in Heleophryne purcelli (Wager, The amount of nuclear DNA is negatively correlated
1965), and presumably more than 1 year in Plectrohyta with the duration of larval development in a wide variety
glandulosa (Duellman, 1970). Tadpoles of the South Af- of anurans (O. Goin et al., 1968). The amount of DNA
 Larvae
! B positívely correlated with metabolic acüvity. Thus, spe- schools based on biosocial attraction. Beiswenger (1975) 169
I fíes that have higher metabolic acüvity have shorter larval classified tadpole aggregations according to their func-
periods. tional characteristics.
Therefore, the rate of larval growth and duration of Aggregations of tadpoles in shallow parts of ponds by
lie larval stage is influenced by a number of intrinsic day apparentíy are the result of individual tadpoles' re-
1 (DNA contení, metabolic rate, yolk reserves) and extrin- sponding to temperature gradients in the water. Experi-
' se factors (temperature, food, inhibitory compounds), as ments by Brattstrom (1962) showed that aggregations of
«cll as absolute size to be reached at metamorphosis. In tadpoles actually raised the temperature of surrounding
nost amphibians, especially anurans, females are larger water. However, the diel cycle of tadpoles of Bu/o amer-
1 fian males. In some cases the larger size may be attained icanas is more directly correlated with changes in light
i by females' utilizing more time from metamorphosis to rather than temperature (Beiswenger, 1977); the imme-
. sexual maturity. On the other hand, in those, as well as diate importance of light probably has evolved through
i apecies in which both sexes require about the same amount the relatíon between light and temperature. Usually an
oí time to reach sexual maturity, larvae metamorphose increase in light intensity in a shallow pond will be fol-
at different sizes. It is not known if the larger larvae are lowed closely by an increase in temperature. Quite pos-
destined to become females. sibly, aggregations of tadpoles of other species also re-
spond primarily to light, as noticed in Agalychnis callidiyas
(Duellman, 1970).
SOCIAL BEHAVIOR Aggregations of metamorphosing individuáis are com-
The kinds of cues and responses existing among larval mon in species of Scaphiopus (Bragg, 1965) and Bu/o
amphibians are poorly known. Although aggregative be- (Beiswenger, 1975; Amold and Wassersug, 1978; G. Zug
havior in anuran larvae has been known for severa! years, and P. Zug, 1979). Metamorphic synchrony in these spe-
few observations are available for salamanders. cies may have evolved as a defense against predation at
metamorphosis, a time when anurans are especially vul-
Salamanders nerable to predation. Presumably this synchronous meta-
Size-dependent spacing behavior is known to occur in morphosis satiates predators and results in higher survi-
larval and neotenic Ambystoma (J. Taylor, 1983). How- vorship than if metamorphosis were asynchronous.
ever, most aggregaüons of larval salamanders seem to The sibling relationships of tadpoles in these obser-
result from the diminution of the aquaüc habitat; larvae vations are not known, but recent experiments with Bu/o
simply congrégate in áreas of remaining water or mois- americanus (Waldman, 1981) and Rana cascadae (Blau-
ture. Aggregaüons of 10 to 50 larvae of A. íi'gn'num were stein and O'Hará, 1981) show that tadpoles recognize
observed in shallow water in a montane pond in Wyo- their siblings and tend to associate with them rather than
ming (Carpenter, 1953); when these aggregations were with nonsiblings.
disturbed, individual larvae scattered, only to reform in Moving schools of tadpoles have been observed in
a few minutes. Similar aggregations of this species have Rhinophrynus dorsa/is (Stuart, 1961), Scaphiopus bom-
been interpreted as feeding aggregaüons (Gehlbach, 1968), bifrons (Bragg, 1965), Scaphiopus ho/brooíd (Richmond,
but there is no evidence that the individuáis in these 1947; Bragg, 1968), Leptodacty/us ocellatus (Vaz-Fer-
groups are attracted to any particular food source or that reira and Gehrau, 1975), Bu/o americanus (Beiswenger,
individuáis benefit from association with other larvae. Ag- 1975), Schismaderma carens (van Dijk, 1972), Hy/ageo-
gregations of metamoiphosing individuáis of A. macro- graphica (Duellman, 1978), Osteocephalus taurinus
dacíy/um (J. Anderson, 1967) may be in response to (Duellman and Lescure, 1973), Phy//omedusa vaillanti
environmental conditions instead of metamorphic syn- (L. Branch, 1983), Pyxicepha/us adspersus (van Dijk,
chronization that might result in greater survivorship of 1972), Rana cascadae (O'Hara and Blaustein, 1981),
young in the face of predation. and Phrynomerus annectens (Channing, 1976).
Essentially stationary schools of tadpoles have been
Anurans observed in two species that are midwater filter-feeders—
Tadpoles of many species of anurans are known to be Xenopus laevis (Wassersug and Hessler, 1971) and Phyl-
gregarious. Aggregations of tadpoles have been inter- lomedusa tarsius (Duellman, 1978). In these tadpoles,
preted as simple feeding aggregations, metamorphic ag- groups maintain their midwater positions by constantly
gregations, clusters in response to environmental gra- fluttering the tips of the tails while body axes remain
dients, and social schools. Since the review and parallel to one another.
classification of social behavior of tadpoles by Lescure Schooling behavior has been interpreted as a mech-
(1968), new observations and experiments suggest some anism to avoid predation or to enhance feeding. Cer-
highly organized social interactions among some kinds of tainly individuáis in large aggregations would be less vul-
tadpoles. Wassersug (1973) classified tadpole aggrega- nerable to predation by small potential predators, such
tions into two broad categories—simple aggregates based as insects and small fishes, than they would be as indi-
on biotaxis other than biosocial mutual attraction and viduáis. This notion has been documented in Scaphiopus
LIFE HISTORY
170 bombifrons, in which Black (1970) observed that the tad- in the presence of artificial light the schools remained
poles only aggregate in the presence of predaceous can- intact (L. Branch, 1983). However, schools of other mid-
nibalistic congencrs or hydrophilid beetle larvae. Avoid- water filter-feeders (e.g., Rhinophrynus dorsalis, Phyllo-
ance of predation by aggregatíve behavior in tadpoles of medusa tarsius) and at least some bottom-feeders (e.g.,
Leptodactylus ocellatus is enhanced by the presence of Osteocephalus taurinus and various Bufo) maintain their
the mother with the tadpoles; she attacks potential preda- integrity at night, presumably by stímuli other than visión.
tors, such as birds (Vaz-Ferreira and Gehrau, 1975). Species-specific selectíon of substrato patterns by tad-
However, gregariousness in shallow water can result in poles of Rana aurora and R. cascadas (Wiens, 1970,
greater vulnerability to predators; Ideker (1976) observed 1972) and experimental evidence that tadpoles of Kal-
high rates of predation on such aggregates of Rana oula pulchra associate with substrate patterns based on
ber/andieri by birds. early experience (Punzo, 1976) suggest that visual cues
Schooling may facilítate feeding. Moving aggregations may be most important in maintaining schools. This may
of Scaphiopus and Bu/o stir up much bottom detritus, be further substantiated by the existence of color visión
thereby creating a rich mixture of suspended particles of in tadpoles (R. Jaeger and Hailman, 1976). Vision may
food (Richmond, 1947; Bragg, 1965; Beiswenger, 1975). be the primary mechanism by which groups of sibling
In moving schools of Osteocephalus taurinus, the tad- tadpoles of Hy/a rosenbergi return to their basin-nest after
poles circuíate within the school so that those at the rear they have been washed out of the nest by high water
of the school move forward along the bottom of the group (Kluge, 1981).
and back along the top (Duellman and Lescure, 1973); However, visión apparently is not an important factor
in this way all individuáis come in contact with the sub- in sibling recognition. Laboratory experiments with tad-
strate, where food is most abundan!. Likewise, circulation poles of Bufo americanus (Waldman and K. Adler, 1979;
of tadpoles within moving schools of B. americanus re- Waldman, 1981) and Rana cascadae (Blaustein and
sults in different individuáis' being at the leading edge O'Hara, 1981; O'Hara and Blaustein, 1981) have dem-
(Beiswenger, 1975). Groups of midwater filter-feeding onstrated conclusively in these species, both of which
tadpoles utilizing parallel orientaüon may genérate more aggregate in nature, that siblings preferentially associate
currents than individuáis do; consequently they increase with one another rather than with nonsiblings. Postem-
the flow of suspended food particles. This idea is sub- bryonic experience with conspecifics is not a prerequisite
stantiated by the fact that weights of tadpoles of Xenopus for sibling preference, because tadpoles of both species
laevis at metamorphosis were positively correlated with raised in isolation later preferentially associated with un-
the densitíes at which they had been raised (Katz et al., familiar siblings over unfamiliar nonsiblings. However,
1981). Also, tadpoles of Rhinophrynus dorsaüs raised in tadpoles of both species that were reared with siblings
isolation grew at a slower rate than those raised in groups and nonsiblings did not show preferential associatíon,
(Foster and McDiarmid, 1982). whereas tadpoles raised only in the presence of siblings
The mechanisms of tadpole schooling have been in- subsequently showed a preferential associatíon with sib-
vestigated experimentally by Wassersug and his associ- lings instead of nonsiblings. Tadpoles of B. americanus
ates (Wassersug and Hessler, 1971; Wassersug, 1973; raised in isolation later preferentially associated with full
Wassersug et al., 1981; Katz et al., 1981; Breden et al., siblings and maternal siblings over paternal siblings. These
1982). These studies have shown that tadpoles of various findings strongly suggest that tadpoles recognize siblings
species can and do orient visually but that other cues also by some innate mechanism and that the mechanism of
are important, at least in some species. For example, recognition may be olfactory. Tadpoles of R. cascadae
tadpoles of Xenopus laevis show parallel orientation in reared in groups from different clutches showed no pref-
both light and darkness, but in light the uniformity of erential associatíon with siblings, whereas tadpoles raised
orientation is greater; also distances between individuáis only with siblings and later placed in mixed groups pre-
are less in darkness than in light. These observations sug- ferentially associated with siblings. Thus, tadpoles raised
gest that orientation is maintained by input into the lat- in mixed groups might assimilate and temporarily retain
eral-line system in darkness and that this is augmented an "odor" of a composite group and be unable to dis-
by visión in light. Different sizes are included in the same tínguish siblings. Preferential association with maternal
schools, except that in Xenopus parallel orientation is over paternal half-siblings in B. americanus suggests that
better developed in larger tadpoles and the distances be- the recognition factor is contributed by the mother. Pos-
tween individuáis is proportional to their size. sibly this factor (pheromone or metabolite) is associated
The results of these experiments partly confirm obser- with the egg capsules; the attractíon to any substance in
vations in nature. Vision seems to be the primary mech- the egg capsules may be enhanced by the continued
anism for schooling in tadpoles of Phrynomerus annec- association of recently hatched tadpoles with the cap-
tens, for the tadpoles scatter at night and reform by day sules.
(Channing, 1976). Individuáis in schools of midwater fil- Possibly sibling recognition is a phenomenon charac-
ter-feeding tadpoles of Phyllomedusa uaillanti disperse at teristic of all tadpole aggregations; if so, this may partially
night; experiments involving lights at night showed that explain the association of tadpoles of the same size in
 Larvae
Oseo woodhousü (Breden et al., 1982) and higher degree that undergo rapid development (see Chapter 2). Coin- 171
m parallel orientation among tadpoles of similar sizes in cidence of anuran breeding with high productivity in both
Xenopus laevis (Katz et al., 1981). However, not all ag- temporary and permanent ponds provides larvae with an
fe^úons of tadpoles contain individuáis of only one abundance of food. Because of this resource availability,
JHBL For example, tadpoles of different sizes compose niche overlap among coexisting species can be high and
¡•civsdual schools of Rhinophrynus dorsalis (Stuart, 1961) the competitive interactions weak; thus, predation may
and Phrynomerus annectens (Channing, 1976). Unless be a major regulator of larval density (Wassersug, 1975).
•ere is considerable discrepancy in growth rates, it seems However, many anurans breed in ephemeral ponds, and
«sSkely that all tadpoles in such schools are siblings. desiccaüon of these ponds can be an important regulator
•aidman (1982) suggested that in some situaüons, in- of the abundance of the species, for entire cohorts are
«fciduals in schools may increase their inclusive fitness eliminated.
l$r associating with kin through aposematic advertise- Wassersug (1975) emphasized that the suspension-
•neiit alarm signaling in response to predaüon, or kin- feeding habits and mechanisms of anuran larvae were
¡•Éuenced growth regulation. Clearly, there is much to especially well adapted for highly eutrophic waters in sea-
barn about tadpole aggregations—their cause, mainte- sonal environments, habitáis in which most, if not all,
•ance. and effect on survivorship. anurans have free-swimming aquatic tadpoles. More-
over, he noted that the amphibious Ufe cycle of anurans
constitutes one of the few biotic mechanisms for transport
EVOLUTIONARY SIGNIFICANCE of excessive nutrients out of eutrophic bodies of water
OF LARVAE into terrestrial ecosystems.
tetphibians lead two lives—at least, those that have aquatic Salamander larvae are essenüally aquatic equivalents
larvae and are terrestrial as adults have two very different of the adults. They opérate at the same trophic level and
fcres. The larvae and adults differ from one another in undergo comparatively few gross changes at metamor-
ttieir modes of respiration and locomotíon and also in phosis. Thus, salamander larvae probably are most like
tisir diets and feeding—especially anurans. These dif- the larvae of primitive amphibians. The varying degrees
ierences are reflected in the behavior of the organisms of metamorphosis of oblígate neotenic salamanders and
and their responses to environmental factors. By utilizing the facultative neoteny of other species reinforces the
•stx) independent sets of resources, larvae are not in com- structural similarity of larvae and adults. Salamander lar-
petition with adults for food or shelter. vae seem to be evolutionary prisoners, temporarily in-
Therefore, it is obvious that selecüve pressures are quite carcerated in the aquatic environment because of the
áfferent on larvae and adults. For example, two species necessity that the eggs develop there. Of course, many
of tree frogs that Uve in the same montane rainforest salamanders, especially plethodontids, have direct de-
might face nearly the same selective pressures as adults, velopment of terrestrial eggs—not necessarily in asea-
but if the larvae develop in different kinds of aquatic sonal environments, but development taking place in hu-
stuations (e.g., temporary ponds versus torrential streams), mid microhabitats.
flie tadpoles of the two species face highly different prob- On the other hand, the morphologically and ecologi-
tems. One must have a rapid rate of development in cally distinctive anuran larvae represent an adaptive ra-
warm water with a low oxygen content, whereas the other diation for utilization of the aquatic environment. Their
must be able to maintain its position and feed in cool, diversif¡catión, which goes back at least to the Cretaceous
flowing water. Both larvae and adults must be successful (Nevo, 1968) and probably to the Triassic (Estes and
in order for the species to survive. Reig, 1973), probably has been an important part of the
Most amphibians, especially anurans, that have aquatic overall radiation of anurans. Thus, the coevolution of
larvae are r-strategists, in that they have many offspring anurans and their larvae is unique among the vertebrales.
 CHAPTER 7
metamorphosis is commonly
tmisioned as ... a long-tailed, round-
mtouthed, fat-bodied polliwog swimming
jfcggís/i/y among vegetation ofa pond and
Aen undergoing extensive alteralions
wohoul any interruption to business to
Secóme a tailless, pop-eyed, insect-eating
forticipant in long-distance jumping
cantes ts.
W. Gardner Lynn (1961)

A Llthough ontogenetic metamorphosis occurs in many

groups of animáis, it is best known in insects and am-
ENDOCRINE CONTROL
Throughout the stages of metamorphosis there is a finely
phibians. Metamorphosis can be defined as a series of tuned integraüon of the endocrine glands, the producís
abrupt postembryonic changes involving structural, phys- of which influence the morphological and physiological
íoiogical, biochemical, and behavioral transformations. changes (Table 7-1). Gundernatsch (1912) discovered
Recent summaries of amphibian metamorphosis are by that metamorphosis in tadpoles of Rana temporaria was
Gilbert and Frieden (1981) and Fox (1984); earlier im- precipitated by feeding the tadpoles on thyroid glands of
portant reviews are by Etkin and Gilbert (1968) and M. horses. This observatíon marked the beginning of the
Dodd and J. Dodd (1976). Three major kinds of changes science of experimental endocrinology and the initiation
occur during amphibian metamorphosis: (1) regression of studies of the endocrine control of amphibian meta-
of structures and funcüons that are significan! only to the morphosis.
larvae; (2) transformatíon of larval structures into a form Nearly all of the experimental work on amphibian
suitable for adult use; and (3) development of structures metamorphosis has dealt with only three species of anu-
and funcüons de novo that are essential to the adult. rans: Xenopus laevis, Rana catesbeiana, and R. pipiens.
Three metamorphic stages defined by Etkin (1932) are Far less extensive studies have been with the salaman-
referenced commonly by experimental biologists: (1) ders Ambysíoma graci/e and A. tigrinum, and the anu-
premetamorphosis, characterized by considerable growth rans Bufo bufo and R. temporaria. Consequently, real-
and development of larval structures but not metamor- istic comparisons among taxa are not possible. The material
phic changes; among amphibians this phase is unique to presented here is only a brief synthesis of the extensive
anurans; (2) prometamorphosis, a period of continued experimental work on the hormonal control of amphibian
growth, especially of limbs, and initiation of minor meta- metamorphosis. Much more comprehensive coverage is
morphic changes; and (3) climax, the period of radical presented by M. Dodd and J. Dodd (1976) and A. White
changes that culminate in the loss of most larval char- and Nicoll (1981).
acters; in anurans the beginning of this period is marked
by the initiation of tail regression, and complete resorp-
tion of the tail marks the end of the period. All of the Thyroid
events of larval growth and metamorphosis are controlled Because of the obvious action of its products on meta-
ulümately by hormones. morphosis in experimental animáis (Table 7-2), the thy-
173
LIFE HISTORY
174 roid commonly is considerad to be the keystone of am- rounds the follicular cavity. The thyroid increases in size
phibian metamorphosis. The primary producís of the during larval development, both by the proliferatíon of
thyroid are two hormones—tetraiodothyronine (T4, thy- follicles and by an increase in the volume of the enüre
roxin) and triiodothyronine (T3). The paired thyroid glands follicle. Both T3 and T4 are made and stored within the
are composed of aggregates of spherical, cystlike follicles. thyroid gland. Synthesis of both hormones occurs by the
Each follicle is lined with a secretory epithelium that sur- iodination of tyrosine residues that are present on a spe-

Table 7-1. Endocrine Levéis and Their Shifts During Amphibian Metamorphosis
Prometamorphosis
Structure or factor Premetamorphosis Early Late Climax
Brain (hypothalamus)
Median eminence Undeveloped Developing Well developed Fully developed
Producüon of TRH None Slight Great Great
Aminergic fibers Undeveloped Developing Well developed Disappear
Effect on prolactin None Slight inhibition Increased inhibition None
Effect on TSH None Slight enhancement Increased enhancement None

Pituitary secretions
Prolactin High Decreasing Low Surge followed by
maintenance of
steady low leve!
TSH Low Increasing High High until end of climax

Thyroid hormones (T3, T4)

Rate of secretíon Low High High High
Plasma levéis Low Low High Low

Interrenal steroids
Aldosterone Low Low Low Increase to adult level
Corticosterone Low Increasing High Decreases, then surges
to adult level
Cortísol Low Slowly increasing Rapidly increasing High, then drops to
adult level

Table 7-2. Major Morphological and Functíonal Changes Induced by Thyroid Hormones During Amphibian Metamorphosis*
Skin Growth of cerebellum
Formatíon of dermal glands Growth of lateral motor column cells
Degeneration of skin on tail Growth of hypothalamic nucleus preoticus
Proliferation of skin on limbs Development of hypophysial portal system and median
Formation of skin "window" for forelimb (anurans) eminence
Degeneratíon of operculum Increase in retinal rhodopsin
Formation of nictitating membrane Fusión of intemal and extemal retinas
Differentíation of Leydig cells Growth of dorsal root ganglia
Sodium transport (? indirect) Degeneration of Rohon-Beard cells
Changes in skin pigments and pigment patterns
Kidney
Connectíve and supportive tíssues Resorption of pronephros
Degeneratíon of tail (anurans) Induction of prolactin receptors
Degeneratíon of gilí arches
Restructuring of mouth and head Respiratory system
Calcification of skeleton Regression of gills

Másele Gastrointestinal tract and associated structiures

Degeneratíon of caudal muscle (anurans) Regression and reorganization of intestinal tract
Growth of limb muscles Reduction and restructuring of páncreas
Growth of extrinsic eye muscles Induction of urea-cycle and other enzymes in liver

Nervous and sensory systems

Reduction of Mauthner cells
Growth of mesencephalic V nucleus
*Adapted from A. White and Nicoll (1981).
 Metamorphosis
tifie protein, thyroglobulin. When the thyroid gland is Interrenals 175
dfenulated to produce thyroid hormones, T3 and T4 are Like the thyroid, these small glands, consisting of cords
; wdeased from the large thyroglobulin molecule and move of cells surrounded by connective tissue and lying under
Mo the bloodstream. the dorsal aorta, also undergo ultrastructural changes
Amphibians, like other organisms, acquire iodine solely during development. For example, in Xenopus laevis the
fcom dietary sources. As metamorphosis proceeds, cer- interrenal tissue apparently is inactive during premeta-
| «En histological changes occur within the thyroid gland. morphosis but shows an increase in activity through pro-
| The secretory epithelial cells become progressively more metamorphosis, reaching a peak at early metamorphic
| «okimnar, reaching a peak at metamorphosis, only to climax and then regressing (Rapóla, 1963). Three inter-
aegress in adults. Furthermore, during metamorphosis the renal steroids have been identified by radioimmunoassay
Asroid gland in anurans undergoes an increase in the in serum of tadpoles of Rana caíesbeiana (Krug et al.,
; atnount of rough endoplasmic reticulum and Golgi ap- 1978). Aldosterone is first detectable in premetamor-
faratus—changes presumably associated with the syn- phosis and remains at a low level until completion of
jfcesis and secretion of thyroid hormones. metamorphosis, when it occurs at the slightly higher level
There is an apparent surge in the production of all characteristic of adults. Corticosterone is present at a low
Éiyroid hormones at metamorphic climax (Stages 41-44) level during late premetamorphosis and rises rapidly in
«Rana catesfaeiana (A. White and Nicoll, 1981). How- early prometamorphosis to reach a peak at about Stage
«wcr, in Xenopus laevis, the level of T4 rises gradually 40; the level declines somewhat to midclimax and then
fcotn late premetamorphic stages to a peak at midclimax; increases rapidly to the concentration occurring in adults.
T3 is not detectable until late prometamorphosis, reach- Corüsol is present in small amounts in early premeta-
ing a máximum earlier than the peak of T4 (Leloup and morphic stages and increases slowly until midprometa-
Buscaglia, 1977). Likewise, in Ambystoma gracile levéis morphosis, from which point there is a rapid increase to
of T4 are greater in metamorphosing animáis than in lar- midclimax and then a decline to the low concentrations
vae or transformed individuáis (Eagleson and McKeown, characteristic of adults. Not surprisingly, the results of
1978). These conclusions are all based on measurements radioimmunoassay of serum of Rana indícate earlier pro-
by radioimmunoassay of the relative amounts of plasma duction of steroids than was suspected originally from
protein-bound iodine, T3, and T4 in the blood. histological examination of interrenals in Xenopus. It is
Several reasons could account for the observed tem- likely that the sensitive radioimmunoassay procedure more
poral differences in circulatory hormone levéis among accurately reflects the synthetic capabilities of the inter-
these species. For example, undoubtedly there is a lag renal glands.
(fcne between the actual secretion and subsequent bind- The activity of the interrenal cells can be stimulated by
mg of thyroid hormones, the extent of which may vary adrenocorticotropic hormone (M. Dodd and J. Dodd,
Étferspecifically. Moreover, in many cases circulating 1976), thereby suggesting that the activity of these glands
plasma levéis of hormones do not accurately reflect intra- is under the control of the pars distalis of the pituitary.
ceEular concentrations. Cells apparently retain T3 better The exact influence of interrenal steroids on metamor-
(han T4 as evidenced by the fací that in target cells, T3 phosis is unknown. The rise in corticosterone levéis dur-
binding to cytoplasmic receptor proteins is about 250 ing prometamorphosis is associated with regression of the
imes greater than binding by T4 (Kistler et al., 1977). intestine, which is induced by thyroid hormones. The
Consequently, it has been proposed that the actual role profile of cortisol levéis in serum coincides with the pat-
of intracellular receptor molecules for thyroid hormones tern of growth of the hindlimbs in Rana catesbeíana, and
in amphibian larval üssues may be to ensure adequate the peak level of cortisol is associated with the beginning
retention of T3 by the cells during metamorphosis. Un- of rapid resoiption of the tail. Because interrenal steroids
fortunately, attempts to explain the observed differences presumably act synergistically with thyroid hormones to
in potencies between T3 and T4 in amphibians by promote tail regression, it has been suggested that cortisol
measured differences in receptor binding have not led to and corticosterone facilítate thyroid-induced metamor-
consisten! results. Apparently the sensitivity of tissues to phosis.
thyroid hormones changes during development. Cells that
once were less responsive to T4 may gradually (or ab- Adenohypophysis
ruptly) acquire the ability to respond (Le., bind) to this The anterior lobe or pars distalis of the pituitary is the
hormone. Such changes unquestionably play an impor- source of many hormones. The secretions that are active
tant role in the ability of a tissue to complete the process during larval development and metamorphosis are hor-
of metamorphosis. Why tissues respond to the various mones that stimulate other endocrine glands or promote
thyroid hormones in different ways and at different times growth. Prolactin and possibly a growth hormone seem
is not clear. Perhaps insights into the control of meta- to direct growth and development by acting on peripheral
morphosis may be obtained by better understanding how endocrine organs and by controlling the activity of the
cells selectively bind T3 and T4 to intracellular receptor thyroid gland. There is disagreement as to whether both
molecules. prolactin and a growth hormone are present in amphib-
LIFE HISTORY
176 ians. it has been suggested that a single hormone with water. However, in contras! to the clear prolactin-thyroid
prolactin- and growth hormone-like properües acts as the antagonism that exists in íhe melamorphosis of larvae lo
somatotropic agent in larval amphibians. Generally, this subadults, there is no consistent evidence for a prolactin-
hormone is referred to as amphibian prolactin. thyroid synergism in the control of the second metamor-
Although the evidence for a somatotropic role of pro- phosis in newts (M. Dodd and J. Dodd, 1976).
lactin among difieren! species is not consistent, indirect The pituitary control of the thyroid gland is accom-
but compelling evidence exists that an endogenous pro- plished by thyroid-stimulating hormone; this hormone in
lactin-like hormone is responsible for suppressing meta- Rana catesbeiana, as in other vertebrates, is a glycopro-
morphosis in Ambystoma, Bufo, and Rana. Prolactin ap- tein (MacKenzie et al., 1978). The early development of
parently is a potent anabolic and somatotropic agent in the thyroid in larval amphibians seems to be partially
specific tissues (e.g., caudal tissue in tadpoles and gills in independent of the pituitary. The follicular arrangement
salamander larvae), but it may do little to drive general in the thyroid epithelium develops in late embryonic stages
metabolism in a direction most suitable for overall growth. independently of pituitary stimulation. The onset of thy-
Perhaps, as suggested by Frye et al. (1972), there is a roglobulin and thyroid hormone synthesis, which first oc-
selectivo advantage provided by the employment of a curs in late embryonic stages, also is independent of thy-
hormone that promotes growth in certain tissues but does roid-stimulating hormone. However, this changes in early
not mobilize importan! energy stores, such as fat bodies, larval stages when normal thyroid function first shows
for the promotion of body growth, because growth is signs of dependence on thyroid-stimulating hormone.
followed by a considerable expenditure of energy for The developmental pattern of pituitary-controlled thy-
structural transformation. Prolactin may favor growth in rotropic activity during the larval period is not so well
larval amphibians by stimulation of intestinal absorption delineated as the developmental changes in the thyroid
of amino acids and glucose. gland itself. In Xenopus laevis, a high level of thyroid-
Prolactin antagonizes the actions of thyroid hormones stimulating hormone occurs during early climax, and the
in certain larval organs. For example, prolactin reduces level declines by midclimax (M. Dodd and J. Dodd, 1976).
tail regression and antagonizes thyroid promotion of This decline correlates with the sharp rise in circulating
hindlimb growth, gilí regression, water and sodium loss thyroid hormone (T3) observed by Leloup and Buscaglia
in certain larval tissues, and nitrogen excretion (A. White (1977). Measurements of thyroid-stimulating hormone
and Nicoll, 1981). However, prolactin does not inhibit correlate directly with the observed changes in activity of
several other responses to thyroid hormones, including thyrotropic cells; also, this activity generally is associated
pancreatic resorption, increased urea-cycle enzymes, he- with changes in the function of the thyroid gland during
patic dehydration, or retinal dehydrogenase activity. Fur- metamorphosis. The action of thyroid-stimulating hor-
thermore, prolactin also may exert a direct inhibitory ac- mone may be confounded by thyroid response to other
tion on the thyroid gland. Because metamorphosis pituitary hormones, especially prolactin. The thyroid and
proceeds at the expense of growth, it might be expected pituitary act in cióse association, and there is a direct
that antimetamorphic and growth-promoting actions of negative feedback of thyroid hormone on the synthesis
hormones are intimately related. There is no evidence and/or secretion of thyroid-stimulating hormone by the
for the separation of these actions. Prolactin antagonizes pituitary.
the action of thyroid hormones at the level of the target The adenohypophysis secretes another substance,
organ. This organ specificity of prolactin antagonism may adrenocorticotropic hormone (ACTH). As mentioned
be an importan! factor in determining the correct se- previously, this hormone stimulates the activity of the
quence and rate of tissue regression or differentiation interrenal glands.
during metamorphosis.
The pituitary gland of amphibians, like all vertebrates, Hypothalamus
is directly controlled by the hypothalamus in the brain. Ultimately, it is the hypothalamus within the brain itself
Dopamine, secreted by the hypothalamus, is a regulator that controls the reléase of pituitary hormones. Within
of prolactin secretion. Dopamine lowers circulating levéis the paired preoptic nucleus of the hypothalamus are a
of prolactin and therefore accelerates metamorphosis in number of neurosecretory cells. These cells are the source
larval amphibians. There is evidence for an inhibitory of small peptides, which function as pituitary releasing
effect of a dopamine agonist on prolactin secretion in the (or inhibiting) factors, and hormones of the neuro-
viviparous Nectophrynoides occidentalis (Zuber-Vogeli, hypophysis, such as oxytocin and vasotocin. Axons ori-
1968). It has been suggested that aminergic fibers reg- ginating within the preoptic nucleus termínate either in
úlate (possibly by tonic inhibition) the reléase of prolactin the median eminence of the hypothalamus or in the neu-
during prometamorphosis; the surge of prolactin secre- rohypophysis of the pituitary gland. Hypothalamic re-
tion in late climax may be caused by reléase from the leasing factors enter the hypophysial portal system by
inhibitory influence of these fibers, which regress at the way of an arterial plexus within the median eminence.
onset of metamorphic climax. Once in the hypophysial portal system, releasing factors
Newts (Notophtha/mus and Tn'turus) undergo a sec- are transported directly to the adenohypophysis.
ond metamorphosis when the terrestrial efts return to There seems to be a clear-cut developmental sequence
 Metamorphosis
• establishment of hypothalamic-piruitary control. In probably by preventing mobilization of the salts and 177
Matapus hevis neurosecretory neurons appear during thereby ensuring an adequate supply of calcium for cal-
t larval stages (Goos, 1978), at about the same time cification during metamorphosis. Relationships of the ul-
t Éte thyroid epithelium assumes a follicular arrange- timobranchial bodies to other endocrine glands have not
The median eminence in Rana pipiens begins to been clearly established; possibly there is a prolactin-
in early prometamorphosis. During late pro- ultimobranchial relationship.
ohosis capillary connection is made with the pars
(Etkin, 1968). Thus, in the case of the thyroid Other Glands
ultímate activation of thyrotropic activity requires Evidence is contradictory concerning the possible role, if
isfcnulus from the hypothalamus. This stimulus is thy- any, of the pineal gland in amphibian metamorphosis.
n-releasing hormone, which acts directly on the Pineal extracts have no effects on metamorphosis of Tar-
to initiate reléase of thyroid-stímulattng hor- icha torosa, Ambystoma tigrinum, and Rana pipiens, but
There is positive feedback between the thyroid accelerate metamorphosis in Bufo amerícartus (M. Dodd
the hypothalamus, because an increase in thyroid and J. Dodd, 1976). If pineal secretions, such as mela-
ífcocnone promotes further development of the median tonin, do have an effect on amphibian metamorphosis,
••inence. As mentioned in the preceding section, the it probably is indirect.
i miction of prolactin is also ultimately controlled by the In addition to the pineal gland, there are metamorphic
¡ bjpothalamus. changes associated with the endocrine páncreas. Differ-
ences in insulin sensitivity and glucose tolerances be-
(Jttimobranchial Bodies tween larvae and adults are related to the action of the
h anurans these glands are paired, but in salamanders endocrine páncreas. Presumably these differences be-
fcere is a single gland. The glands form at the same time come established during metamorphic climax and are
m the operculum (early premetamorphosis). They de- accounted for by hormone-mediated activation or inten-
seiop as thickenings in the floor of the fifth branchial (last sification of insulin-antagonistic functions; changes in
pharyngeal) pouch. Subsequentíy, secretory cells of neural growth hormone and glucocorticoid secretions and their
oest origin migrate into the pharyngeal epithelium. Even- metabolic effects are believed to be responsible for these
teaDy the glands sepárate from the original pouch área changes (M. Dodd and J. Dodd, 1976).
and acquire a definite lumen. At the beginning of meta-
morphic climax the epithelium becomes entirely stratí- Hormonal Integration
ied, and the ultimobranchials increase in size. This period A model for the control of anuran development and ac-
of activity coincides with the period of calcium mobili- tivation of the metamorphic climax proposed by Etkin
zation from the endolymphatic sacs. These sacs are as- (1968) has been modified by M. Dodd and J. Dodd (1976)
áociated with the auditory organs and have posterior ex- and A. White and Nicoll (1981). This model can be out-
tensions along the vertebral column. Calcium carbonate, lined, as follows (Fig. 7-1):
in the form of aragonite, is stored in these paravertebral
"%ne sacs" and in the endolymphatic sacs. During larval 1. During premetamorphosis, the median emi-
Ife, the endolymphatic sacs enlarge. Ultimately the ac- nence of the hypothalamus is undeveloped,
cumulated calcium is utilized at metamorphosis for com- and the brain exerts little or no control over
pletion of the calcification of the skeleton. The ultimo- adenohypophysial functions. Consequently,
branchial bodies and "lime sacs" are retained in most secretion of prolactin is high and secretion of
postmetamorphic anurans, with the exception of Xeno- thyroid-stimulating hormone (and thus thy-
pus laevis (M. Dodd and J. Dodd, 1976). roid hormone levéis) is low. Therefore, pro-
Thus, the ultimobranchial bodies serve to sequester lactin can promote larval growth without in-
calcium salts in special storage sacs during development, terference from thyroid hormones. Negative

-Prolactin (plasma levéis)

£o
Thyroid -stimulating hormone—^..--'''..--'''

Oí Figure 7-1. Hypothetical relative

DC
levéis of pituitary and thyroid
1 hormones in Rana catesbeiana
Premetamorphosis |Early - Prometamorphosis - Late| Climax during metamorphosis.
LIFE HISTORY
178 feedback of thyroid hormone on secretion of fibers disappear during metamorphic climax.
thyroid-stimulating hormone ¡s operative. Thus, rising levéis of thyroid hormones during
2. During early prometamorphosis, the rate of se- late prometamorphosis may act on the hypo-
cretion of thyroid hormone is high, but this is thalamus and cause these fibers to increase
not reflected in increased plasma protein- secretion of thyroid-stimulating hormone,
bound iodine or by radioimmunoassay-de- thereby accounting for the positive feedback.
tectable plasma T3 or T4 levéis, probably be- Rising levéis of thyroid hormones also may
cause of the rapid clearance of the thyroid cause the eventual degeneration of these fi-
hormones. The increased secretion of thyroid bers. Thus, neural stimulation of secretion of
hormones presumably results from rising lev- thyroid-stimulating hormone is lost, and the
éis of thyroid-stimulating hormone; this in- inhibitory action of thyroid hormone directly
crease probably reflects gradual development on the pituitary can opérate unopposed.
of hypothalamic influence on the adenohy-
pophysis. The rate of secretion of thyroid hor-
mones continúes to increase, so that late in OTHER BIOCHEMICAL CHANCES
prometamorphosis the capacity of tissues to The morphological and physiological changes that take
bind and utilize thyroid hormones is satu- place during metamorphosis are accompanied by, if not
rated. Consequently, the continually increas- driven by, nonhormonal biochemical changes. Electro-
ing ourput of thyroid hormones results in a phoretic and radioimmunoassay investigations indícate
surge in plasma levéis of these hormones. that marked changes take place in the blood in late pro-
3. The rising level of thyroid hormones also pro- metamorphosis and during metamorphic climax (Broyles,
motes development of the median eminence 1981), and numerous biochemical changes also occur
and the establishment of portal vascular con- during organ differentiation and maturation (Smith-Gill
nections between the hypothalamus and the and Carver, 1981; Atkinson, 1981). The changes in hor-
adenohypophysis. As this process progresses, mone levéis in the blood have been discussed in the
more thyrotropin-releasing hormone is able preceding section.
to reach the pituitary to stimulate increased
secretion of thyroid hormones. The increase Serum Proteins
in thyroid hormones promotes further devel- One importan! function of serum proteins is to maintain
opment of the median eminence. Thus, a osmotic equilibrium between blood and tissue fluids. An
positive feedback loop is established. increase in the total protein concentration at metamor-
4. While hypothalamic control of pituitary func- phosis serves to increase the osmotic pressure of the blood
tion is developing, secretion of prolactin comes and henee its water-retaining capacity, an important
under inhibitory control, and the circulating adaptive switch considering the transition from the aquaüc
levéis of prolactin decrease progressively. Thus, environment of larvae to the terrestrial environment of
prolactin antagonism of thyroid hormone ac- posrmetamorphic amphibians. Albumin, with its lower
tion on peripheral tissues is reduced, allowing molecular weight, exerts two to three times the osmotic
development to proceed more rapidly. pressure per unit weight in comparison with the globulins.
5. Late in prometamorphosis, the median emi- Not surprisingly, albumin increases proportionately more
nence and its vascular connections with the than globulins during metamorphosis. At normal blood
hypophysis have developed substantially. The pH, albumin has great ion-binding capacity. An increase
saturation of tissues with thyroid hormones in the ion-binding capacity per unit volume of blood at
results in rapid and complete transformation metamorphosis fulfills the greater transport needs asso-
(climax). Blood levéis of prolactin are greatly ciated with metabolism and excretion in the terrestrial
reduced during this period, reflecting máxi- environment (Frieden, 1961).
mum hypothalamic inhibition. Thus, at this The concentration of serum proteins more than dou-
stage of development the prolactin-mediated bles during metamorphosis in various Rana (Just et al.,
inhibition of thyroid hormone action is mini- 1977), and at least 20% of the increase in R. catesbeiana
mized. is due to an increase in serum albumin, which rises more
6. During metamorphic climax, the positive feed- than 10-fold (Feldhoff, 1971). At least part of the increase
back interactions of the hypothalamo-hypo- in serum albumin during metamorphosis is due to an
physial-thyroid axis presumably are lost. It is increased rate of synthesis in late prometamorphosis in
not clear how this comes about. Possibly the R. catesbeiana (Ledford and Frieden, 1973); serum al-
aminergic fibers that "innervate" the adeno- bumin peaks at early climax and declines at late climax
hypophysis in larvae are involved in both the to just about the same level as in midprometamorphosis.
positive and negative feedback loops. These Albumin levéis remain high in froglets, indicating a de-
 Metamorphosis
creased rate of albumin degradaüon. In species of am- the immature, differentiating cells that synthesize hemo- 179
bystomatid salamanders (Nussbaum, 1974), there are in- globin.
oeases in the albumin/globulin ratio and total protein
concentrations. However, in the aquatíc Cryptobranchus Red Blood Cells and Hemoglobins
aieganiensis there are no changes in serum proteins Morphological differences between larval and adult red
Ifückerson and Mays, 1973). blood cells have been noted in numerous species of anu-
The hypothesis that the increase in albumin attendant rans (Broyles, 1981). During metamorphosis, larger lar-
wtíh metamorphosis is designed by natural selection to val red blood cells are replaced by smaller adult red blood
meet the osmoüc needs of the organism in the terrestrial cells; the midpoint of this transition is at midclimax. The
«nvironment (Frieden et al., 1957) was proposed as an red blood cell count and whole blood hemoglobin con-
adaptive aspect of amphibian metamorphosis. Subse- centration are greater in adults than in larvae. The ma-
quent investigations on Bufo arenarum from humid and ture, differentiated red blood cell retains its nucleus in
and habitáis (Bertíni and Cei, 1960) and various ambys- both larval and adult blood cells, but the nuclei of larval
lomatid salamanders (Nussbaum, 1974) demonstrated cells have a greater amount of endoplasmic reticulum
fíat there is both interspecific (Ambystoma macrodac- than do adult red blood cells.
%,-fum and Rhyacotriton olympicus) and intraspecific (Di- Differences in the nuclei and cytoplasm support the
amptodon ensatus and B. arenarum) evidence that higher view that adult red blood cells are more mature cells and
concentrations of albumin are characteristic of trans- less active in the synthesis of amino acids and proteins,
formed individuáis of populations adapted to more arid as compared with larval red blood cells. Circulating red
«nvironments. blood cells of premetamorphic tadpoles of Rana cates-
The absence of metamorphic changes in serum protein beíana and R. pipiens have a greater ability than the red
concentrations in Cryptobranchus is understandable. blood cells of froglets or adults to incorpórate amino acids,
However, the aquatic Xenopus laevis exhibits a marked uridine, and thymidine (Benbassat, 1970). Thus, there
change in albumin/globulin ratio and total protein con- are both morphological and biochemical differences be-
eentration between larvae and adults. In comparison with tween larval and adult red blood cells. Of course, of ma-
Rana, this change is slow and steady and continúes after jor importance is the difference in the types of hemoglo-
noorphological metamorphosis. The differences between bins that they contain.
Roña and Xenopus are reasonable in that a rapid change A notable transition in hemoglobins takes place at
in serum proteins in Rana is necessary for the froglet to metamorphosis. Extensive work on Rana catesbeiana
survive in the terrestrial environment, whereas Xenopus (Frieden, 1968) ¡Ilústrales the adaptive significance of the
remains aquatic. Then, why should concentrations of transition. Hemoglobins of tadpoles have higher affinities
serum proteins change in Xenopus and not in Crypto- for oxygen and are well suited for an aquatic environ-
branchus? The latter lives in permanent rivers, whereas ment where oxygen tensions are low. Adult hemoglobins
Xenopus lives in ponds that may dry up during droughts; have a lower affinity for oxygen. Although it requires a
the frogs aestivate in the soil during droughts and thus greater oxygen tensión to load the adult hemoglobins,
are confronted with the osmoregulatory demands faced they will reléase oxygen more readily at the oxygen ten-
by terrestrial frogs such as Rana. sions that prevail in the various tissues of the animal.
Thus, adult hemoglobins are well suited for an air-breath-
Iron Transport, Metabolism, and Storage ing animal that requires a more active metabolism to
Ceruloplasmin is the principal copper protein of serum support its greater muscular activity.
and is important in donating copper to cells for the syn- The four major hemoglobins (I-IV) in tadpoles of Rana
thesis and assembly of cytochrome oxidase; also it is a catesbeiana are different from the four major hemoglo-
molecular link between iron and copper metabolism. The bins (A-D) in adults. The change from one set to another
ferroxidase activity of ceruloplasmin is important in the occurs during larval life. In early premetamorphic larvae,
mobilization of iron from fem'tin, an intracellular iron- about 90% of the total hemoglobin is made up of com-
storage protein. Levéis of ceruloplasmin increase grad- ponents I and II, whereas in late premetamorphic stages
ually through premetamorphosis and rapidly during pro- about two-thirds of the hemoglobin is composed of com-
metamorphosis to peak at the beginning of metamorphic ponents III and IV (Broyles, 1981). Of the four adult
ctimax in Rana gry/io (Frieden, 1968). There is a signif- hemoglobins, A and D are relatively minor, and com-
icant increase in ferritin reducing activity in the liver in ponent C has a higher oxygen affinity than B. Compo-
early metamorphic climax (Osaki et al., 1974), which nent C is the first to appear during metamorphosis and
undoubtedly plays a role in the mobilization of iron from comprises essentially all of the hemoglobin in froglets.
the liver. The marked increase in ceruloplasmin is prob- In Rana catesbeiana the switch in hemoglobins occurs
ably important in mobilization of iron from both the liver rapidly, mostly in midclimax, but some adult hemoglobin
and larval red blood cells and the transfer of iron to serum is detectable in late prometamorphic stages. Similar
transferrin. Transferrin is required as a donor of iron to hemoglobin transitions are known in several other spe-
LIFE HISTORY
180 c¡es o{ píana (Broyles, 1981). The hemoglobin transiüon ogy (type 1) containing larval hemoglobin (type
begins much earlier and ends much later in Xenopus IV).
laevis (Maclean and Jurd, 1971) and especially in Bom- 3. Liver erythropoiesis begins in early premeta-
bina variegata (Cardinelli and Sala, 1979). The lengthy morphic stages in Rana pipiens and continúes
duration is understandable in Xenopus, adults of which through metamorphosis in R. catesbeiana. In
are aquaüc. The functional significance of the lengthy R. pipiens macrophages are the predominant
period of transitíon in Bombina is unknown, but it simply hemopoietíc cell type in the liver in early pre-
may represent a primitive condition of prolonged meta- metamorphic stages, and erythroblasts dom-
morphosis. inate in midpremetamorphic stages. It is not
Three major types of hemoglobin have been identified known whether mesonephric kidney eryth-
in larvae and three others in adults of the salamander ropoiesis and liver erythropoiesis begin si-
Dicamptodon ensatus (S. Wood, 1971). The ontogenetic multaneously or at different developmental
changes in hemoglobins in Dicamptodon are similar to stages. In tadpoles of R. catesbeiana liver
those in anurans with respect to oxygen affinity. The tran- erythropoiesis produces red blood cells that
sitíon from larval to adult hemoglobins occurs at the time differ in cell morphology (type 2) and hemo-
of morphological metamorphosis in Ambystoma ti- globin type from red blood cells emanating
grinum; a similar transitíon occurs at about the same age from the kidneys.
(100-150 days) in the neotenic A. mexicanum but is not 4. As development progresses toward metamor-
accompanied by morphological metamorphosis (Duci- phosis in R. catesbeiana, the relative contri-
bella, 1974). butíon of the kidneys and liver to total eryth-
A distínctly different kind of ontogenetíc shift in oxygen ropoiesis changes—kidney erythropoiesis
equilibrium has been described for the aquatíc, vivipa- predominates at earlier stages, whereas liver
rous caecilian Typhhnectes compressicauda (Garlick et predominates at later stages.
al., 1979). Developing fetuses of this species have large 5. During metamorphic climax in R. catesbeiana,
external gills (Fig. 5-6) that function in gaseous exchange liver erythropoiesis switches from production
with maternal oviducal tissue. Oxygen affinity of fetal blood of larval to adult hemoglobins. Presumably
is higher than that of adult blood, but the hemoglobins kidney erythropoiesis declines. The molecular
of fetuses and adults are essentially the same structurally and cellular events that occur in the liver to
and have the same oxygen-binding capacities. The dif- medíate the metamorphic switch in hemoglo-
ferences in binding properties are the result of a three- bins are largely unknown. There is disagree-
fold increase in the level of adenosine triphosphate in the ment as to whether both larval and adult
blood of adults. hemoglobins occur in the same red blood cells
A general scheme of changes in erythropoiesis and during the transition.
hemoglobin synthesis during anuran development was 6. In froglets the liver is the primary erythropoietic
presented by Broyles (1981), as follows: site. The red blood cells produced there are
uniform morphologically and apparently con-
1. The first red blood cells arise in the ventral tain only adult hemoglobins. However, there
blood islands of the embryo. The type of may be a low level of larval hemoglobins in
hemoglobin synthesized in these embryonic the circulating blood of froglets and adults.
red blood cells is unknown. 7. During maturation of the froglet into an adult,
2. Both pronephric and mesonephric kidneys are erythropoiesis shifts from the liver to one or
erythropoietically active in larvae and repre- more other sites. Apparently the spleen is the
sent the second ontogenetic site(s) of forma- principal erythropoietic organ in adult frogs.
tion of red blood cells. In Rana pipi'ens the However, in températe species red blood cells
pronephros becomes hemopoietically active also are produced by the bone marrow in the
in early premetamorphosis and is mainly a spring of the year.
granulocyte producer during the larval pe-
riod. Erythropoiesis constítutes less than 10% Liver
of the hemopoietíc actívity of the pronephros The changes in the liver that accompany metamorphosis
in early premetamorphosis. The relative num- encompass a panorama of biochemical differentíation
ber of different types of hemopoietic cells in events. These include DNA synthesis, synthesis and ac-
the mesonephros at different stages of early cumulatton of a stable amount of transcriptional RNA
development is unknown. However, in late with an associated enumeration of nucleoli, lipid synthe-
premetamorphic stages the intertubular re- sis, elaboration of the rough endoplasmic reticulum, and
gions of the mesonephric kidneys are pro- a change in the structure and an increase in the number
ducing red blood cells of a defined morphol- of mitochondria. Newly synthesized proteins include the
 Metamorphosis
enzymes of the ornithine-urea cycle, which develop in Eye 181
association with the transition from ammonotelism to The principal biochemical change in the eye is the con-
ureotelism. Regulation of the rates of protein synthesis versión of photopigments. Two systems of photopig-
seems to be at both the transcriptional and posttranscrip- ments are contained in the reünal rods of amphibians.
íonal levéis. During metamorphosis, periods of DNA Most adult amphibians have rhodopsin, a red-photosen-
synthesis precede the appearance of new proteins, and sitíve pigment in cycle with vitamin A1; and larvae have
cell death may accompany liver metamorphosis. Presum- porphyropsin, a purple-photosensitive pigment in cycle
ably, significan! cellular turnover precedes biochemical with vitamin A2. Each photopigment is a conjugated pro-
(fifferentiation, and differentiation of adult funcüon occurs tein (opsin), containing as the prosthetic group retina^
in proliferating populations of cells. However, a func- or retina!2, which are aldehydes of vitamins A x and A2,
ional relatíonship between proliferation and liver meta- respectively.
morphosis has not been established experimentally. The transition from porphyropsin to rhodopsin occurs
during metamorphosis, and the retinas of parüally meta-
btestine morphosed larvae contain a mixture of the two types of
In anurans regression of the gut occurs during late pro- photopigments. At least one species that is aquatic as an
metamorphosis and metamorphic climax, and is char- adult, Xenopus laevis, retains porphyropsin as the visual
acterized by shortening of the gut and loss of the primary pigment (Bridges et al., 1977). Newts (Notophthalmus
epithelium. This loss seems to be initiated by the mobi- and Triíurus) that undergo a second metamorphosis from
ization of lysosomes and reléase of hydrolases into the terrestrial subadults to aquatic adults have a porphyrop-
cytoplasm of the epithelial cells. Alkaline phosphatase sin-rhodopsin-porphyropsin sequence (Grüsser-Cornehls
activity, which is correlated with a functional larval epi- and Himstedt, 1976). Whether thyroid or one or more
thelium, decreases during regression of the gut. other hormones subsequently induce a particular visual
pigment during metamorphosis is a function of prior evo-
Integument lutionary selection. Depending on the life history of the
Scveral biochemical changes occur in the skin during species, thyroid hormones may coordínate the change in
metamorphosis. Thyroid hormones presumably are re- larval photopigment to that of the adult. However, in
sponsíble for the proliferation of epidermal cells, sodium- newts prolactin has been identified as inducing the change
phosphorus-adenosine triphosphate synthesis, and at least from rhodopsin in terrestrial subadults to porphyropsin
one protein involved in keratínizatíon. Other funcüons of in aquatic adults.
ihe skin, such as osmoregulation, are influenced by pro-
bctin. Development and regulaüon of the active sodium Tail and Gills
transport system may be mediated by different hor- During amphibian metamorphosis the gills and tail (anu-
mones. rans only) undergo complete degeneration. Experimental
During metamorphosis, chromatophore densiües, as- studies (summarized by Atkinson, 1981) of spontaneous
sodations, and morphologies typical of the adult pig- and thyroid-induced anuran gilí and tail atrophy suggest
mentary pattern develop, although additional changes in that degeneration in these organs encompasses at least
pigmentation may occur in later postmetamorphic life. three discrete phases of cellular activity. In the first phase
Complex interactions among pigment cells, their bio- a selective decrease in the rate of protein synthesis oc-
chemical producís, and their tíssue and endocrine envi- curs; the second phase is highlighted by enhanced his-
ronments medíate pattern formatíon and pigment syn- tolytic activity; and in the final phase cellular debris pro-
thesis. Morphological transitíons include migrations and duced during the second phase is eliminated. Each tissue
rearrangements of existing chromatophores, mitosis of of these organs participates in each phase in a charac-
chromatoblasts and existing differentíated chromato- teristic manner.
phores, and differentiation of new chromatophores (Smith-
Gill and Carver, 1981). Pigment synthesis and chromato- Lungs
phore differentiation are essenüal to expression of the In Rana catesbeiana, rates of incorporation of amino acids
color pattern and may involve the production of new and thymidine into the lung tissues increase and their
pigments and/or the development of new organelles. Also, rates of incorporation in the degenerating gilí tissues de-
specific classes of pigments may be degraded. Both thy- crease during metamorphic climax (Atkinson and Just,
roid hormone and melanocyte-stimulating hormone may 1975). It may seem that the lung tissue prepares bio-
be important in the development of the pigmentary pat- chemically to assume a respiratory role before it actually
tern. However, much of the evidence linking thyroid hor- begins its major respiratory function. However, many kinds
mone action with changes in pigment patterns at meta- of tadpoles, including those of R. catesbeiana, swim to
morphosis is circumstantial and is based on the temporal the surface and gulp air when oxygen concentrations of
association of pigment changes with other aspects of the water are low. Thus, biochemical preparation for res-
metamorphosis. piratory function of differentiating lung tissue is necessary
LIFE HISTORY
182 prior to the lungs becoming the major respiratory struc- in late metamorphosis. The internal gills and associated
tures in froglets. blood vessels degenerate; lungs and pulmonary ventila-
tion develop. The tail is resorbed, and the skin thickens
with the development of dermal glands. Larval mouth-
MORPHOLOGICAL CHANCES parts degenerate, and the adult mouth is formed. A tongue
The most obvious changes during metamorphosis are in (except in pipids) and associated hyolaryngeal structures
the structure of amphibians. The changes are most ex- develop. The intestine shortens, and the digesüve tract
tensive in anurans, in which the aquatic larva undergoes differentíates. The eyes enlarge and undergo structural
a drastic transformation into a terrestrial adult. modifications; eyelids develop.
Metamorphosis in caecilians seems to involve the few- In all groups of amphibians, changes occur in the uro-
est changes, but this group has been studied far less thor- genital system. The pronephric kidney degenerates, and
oughly than the others. From the works of P. Sarasin and an opisthonephric or mesonephric kidney forms. The
F. Sarasin (1887-1890), Brauer (1899), H. Marcus (1939), gonads and associated ducts develop. Comprehensive
and E. Taylor (1968), it is possible to summarize existíng summaries of morphological metamorphosis by M. Dodd
knowledge, based mostly on Hypogeophis rostratus and and J. Dodd (1976) and Fox (1981, 1984) are discussed
¡chthyophis g/utinosus. Gilí degeneration occurs during here by organ systems.
late embryonic, larval, or fetal life. In those caecilians
having aquatic larvae, the gills are lost (either by resorp-
tion or breakage) soon after hatching, leaving only a sin- Skeleton
gle gilí slit on either side. Upon metamorphosis the gilí Whereas the appearance of limbs, resorpüon of the tail,
slits cióse. A dorsal caudal fin is present in larval ichthy- and development of eyelids are obvious corollaries of the
ophiids and rhinatrematids; this degenerates during shift from an aquatic to a terrestrial mode of life in anu-
metamorphosis. Sometime during fetal life the eyes of rans, less apparent but no less dramatic changes involve
most caecilians become covered with skin or bone, and the restructuring of the larval skull and hyobranchial ap-
certain muscles and nerves associated with the eyes either paratus. These changes (1) accommodate the transition
do not develop or degenerate. During fetal or larval life, from larval feeding and respiratory modes to those of the
the sensory tentacles develop in front of the eyes. In late adult, and (2) house newly developed sensory organs
stages of metamorphosis, the skin thickens, skin glands that serve the organism's needs in the terrestrial environ-
form, and snnall scales develop in the skin. The lungs ment. Skeletal changes are much less conspicuous in sal-
probably are not funcüonal until after birth, and therefore amanders and caecilians and are discussed in Chapter 6,
metamorphosis also entails lung maturaüon. The fetal which contains a discussion of terminology and illustra-
teeth are lost, and adult dentition develops immediately tions.
after birth. The formation of the adult mouth involves a restruc-
Although the transition from larva to adult is not nearly turing of the anterior end of the chondrocranium and a
so dramatic in salamanders as it is in anurans, definite complete reorganization and realignment of the larval
changes take place during metamorphosis. The morpho- palatoquadrate. The suprarostral cartilage, which sup-
logical changes in salamanders detailed for Eurycea bis- ported the upper beak of the tadpole, disappears along
hneata by I. Wilder (1925) and summarized for salaman- with the distal ends of the cranial trabeculae that sup-
ders in general by M. Dodd and J. Dodd (1976) include ported it. The infrarosrrals supporting the lower beak fuse
locomotor, sensory, respiratory, and feeding structures. with Meckel's cartilage, which is lengthened to accom-
The caudal fin is resorbed, and the skin thickens with the modate the vertical rotation of the quadrate and the pos-
development of dermal glands. Gills are resorbed and gilí terior shift of the jaw articulation (between Meckel's car-
slits cióse; associated branchial circulaüon is modified as tilage and the quadrate) from the región of the olfactory
lungs develop (except in plethodonüds). Eyelids develop, foramen to the auditory capsule. The formation of the
and the simple flap of connective tissue that acts as a adult maxillary arch also involves the disappearance of
valve to cióse the internal nares in larvae may be replaced larval neurocranial braces and the formation of new struts
by a more sophisticated valve operated by smooth mus- to brace the upper jaw against the skull. Thus, the quad-
cle fibers. The larval labial folds shrink, and the mouth ratojugal commissure, ascending process, and larval oüc
takes on a different appearance with a wider gape. Max- process break down. The muscular process of the quad-
illary bones are formed, and teeth develop on the max- rate fuses dorsally with the crista parotíca of the auditory
illaries and parasphenoid. A tongue develops, and as- región by means of the adult oüc process. Posteroven-
sociated changes occur with the hyobranchial apparatus. trally the quadrate is braced against the auditory cap-
Because larval and adult anurans are such divergent sule via the pseudobasal process, a block of cartilage that
organisms morphologically and ecologically, it is not sur- arises beneath the anterior end of the auditory capsule.
prising that the transition from tadpole to froglet is abrupt The pterygoid process lengthens to attach to the devel-
and dramatic. The hindlimbs grow and mature; forelimbs oping nasal capsule anteriorly (via the posterior maxillary
develop in the branchial chambers, from which they erupt process), and the auditory capsule posteromedially.
 Metamorphosis
The ccratobranchials that form the larval branchial articúlate with the first presacral vertebra via the occipital 183
•Ees dísappear as the hyobranchial apparatus assumes condyles.
fe feítened adult shape that serves as a framework for The surprisingly sparse Information on sequences of
• tongue. The first basibranchial is resorbed, whereas ossification in anurans was summarized by Trueb (1985).
• second is incorporated with the hypohyal plates to This is most nearly complete for species of Rana and
BE the corpus or hyoid píate of the adult. The large Xenopus laevis. Because the timing of metamorphosis is
hyals lose their connectíon with the larval palato- highly variable, it is impossible to draft a generalized
ate and become long slender elements (anterior schedule of ossification applicable to all frogs. Thus, in
or hyalae) that extend anterolaterally and then some species, the organism may be quite well ossified
i posteriorly to fuse with the ventral aspect of the before it transforms, whereas in others the greatest part
capsules. of ossification occurs during or after metamorphosis. Os-
kt the ethmoid región, the anterior neurocranial wall sification proceeds cephalocaudally in those species for
•d comua trabeculae undergo an elabórate transfor- which there are data; thus, elements of the skull begin
•Éon that results in the paired nasal capsules composed to ossify before vertebral elements, and limb bones ossify
'<• dfa variety of cartilaginous supports (described in Chap- in a proximodistal sequence. Only the most generalized
•r 13) that protect the olfactory organs. In the larva, the scheme of ossification can be outlined for cranial com-
«eemal naris cannot be closed, and closure of the narial ponents. Usually the first bones to appear before meta-
canal is affected through hydrostatic pressure against a morphosis are neurocranial roofing and flooring elements
«•Vular flap covering the internal choana. This flap is (frontoparietal and parasphenoid) and the exoccipitals,
••ssing in adults, and the narial passage is closed instead which form the back end of the skull. During late pro-
i$r movement of the cartílages supportíng the external metamorphosis and metamorphic climax, the auditory
•ans. Posterior to the ethmoid región, in the orbitotem- área of the braincase (prootic) ossifies along with the roof
poral área, the basicranial fenestra closes and the neu- of the nasal capsule (nasal), the septomaxilla internal to
«xianial walls proliferate so that the optíc and trochlear the nasal capsule, and the upper jaw (maxilla and pre-
aerve foramina are delimited. Depending on the species, maxilla). During the latter part of metamorphic climax,
ifoe pilae antoticae may be united dorsally by the taenia the main elements of the mandible (dentary and angu-
tecti transversalis, and a medial element, the taenia tectí losplenial) appear along with the bracing elements of the
medialis, may connect the transverse tectum to the tec- maxillary arch (pterygoid and squamosal) and the vomer.
lum synoücum posteriorly. Laterally, the eye is protected The last bones to ossify are the mentomeckelians at the
by a saucer-shaped sclerotíc cartilage. mandibular symphysis, the palatine, quadratojugal, col-
In the auditory región, the roof of the otic capsule is umella, and sphenethmoid, which forms the anterior end
proliferated into a lateral extensión, the crista parotica, to of the braincase. As pointed out by Trueb and Alberch
which the quadrate is attached by the otic process. The (1985), those elements that frequently are absent from
fenestra ovalis, which lies ventral to the crista parotica, is the skulls of some anurans (i.e., vomer, palatine, quad-
occluded by two cartilaginous structures that arise inde- ratojugal, and columella) are among the last cranial com-
penden! of the wall of the otic capsule—the operculum ponents to appear.
posteriorly, and the pars interna plectri of the columella
anteriorly. The rodlike columella fuses with the ventral Integument
cdge of the fenestra ovalis and bears two transient liga- Amphibian skin is a dynamic cellular system adapted to
mentous connections—proximally with the operculum and a complex and changing life cycle. The larval epidermis
¡distally with the posterior surface of the quadrate. Even- and dermis are composed of many different cellular com-
tually, synchondrotic connection of the proximal portion ponents, each of which differs in structure, function, and
of the columella with the margin of the fenestra ovalis is topographic relationships; also some kinds of cells differ
replaced with a ligamentous one, and upon ossification in their times of origin and duration of existence. The
the operculum and columella are fused. The tympanic skin becomes progressively more elabórate in its cellular
ring originates from cells derived from the quadrate. Sub- composition as development proceeds. However, some
sequent to metamorphosis it chondrifles and fuses dor- kinds of epidermal cells origínate early in larval life and
sally to the crista parotica; coincidentally, the ring seems disappear prior to prometamorphosis. Other kinds exist
to act as an organizer in the formation of the tympanic throughout larval and adult life. Although the ultímate
membrane. The cartilaginous distal portion of the colu- fate of some specialized cells is unknown, it is likely that
mella (pars externa plectri) extends from the crista par- apart from the germinativo layer, most if not all epidermal
otica to the distal end of the pars interna plectri and fuses cells and much of the dermis ultimately degenerate and
with the latter once the proximal columella has lost its disappear; some of these are replaced regularly through-
ligamentous connection with the quadrate. out life.
In the occipital región, the notochord is incorporated The epidermis proper is formed when the outer epi-
into the basal píate by chondrification and encroachment thelial layers of the skin are delimited by a basement
of the parachordal cartilages, the posterior ends of which membrane. Larval epidermis consists of two or three lay-
LIFE HISTORY
184 ers ofcells; these increase to five or six layers at meta- idenüfied in the epidermis of anuran larvae;
morphic climax. In early larvae the epidermis lies on the cells of the same type occur in the epithelium
thin, unstructured basement membrane and a thicker of the bladder and palate of some adults but
collagenous lamella. In addition to epithelial cells, larval not in the epidermis of adults.
epidermis contains some specialized cells (Table 7-3). 5. Flask cells, which are rich in mitochondria in
These include: adults, first appear in situ in the epidermis at
metamorphic climax.
1. Merkel cells consütute only about 0.3% of the 6. Goblet cells are mucous surface cells known in
number of epidermal cells and have recipro- tadpoles of Xenopus.
cal synapses with nerve termináis; possibly they 7. Mucous surface cells are mucus-producing cells
function as mechanoreceptors. Apparently they that appear in early larval stages and persist
originate from interstitial cells in the epider- after metamorphosis.
mis, and they persist in adults. 8. Ciliary cells develop in embryos and function
2. Leydig cells are specialized epithelial cells that in embryonic movements; some of these per-
probably secrete mucus into subsurface ex- sist as vestiges in early larval stages.
tracellular compartments of the epidermis. Al- 9. Neuromast cells are the sensory cells in the
though they occur in tadpoles, they are far lateral-line system characteristic of all am-
more abundant in salamander larvae. The phibian larvae, aquatic adult salamanders, and
Leydig cells disappear at metamorphosis. adult pipid frogs. The lateral-line organs origi-
3. Stiftchenzellen are possibly chemoreceptor cells nate from pre- and postauditory placodes and
in the epidermis of anuran larvae; they are subsequently migrate and differentiate. Each
unknown in adults and presumably degen- neuromast cell has a surface kinocilium and
erate at metamorphosis. stereocilia. Lateral-line systems are fully de-
4. Mitochondria-rich cells that possibly function in veloped at the time of hatching. Their devel-
osmoregulation or ion transport have been opment has been described for a newt, Cy-
nops pyrrhogaster (Sato and Kawakami,
1976). The changes that take place at meta-
Table 7-3. Cellular Componente of Skin in Larval and Adult morphosis in Xenopus laevis affect the his-
Amphibians" tology and innervation of the neuromast cells
Larva6
(Shelton, 1970). In Xenopus, the individual
Adult sensory plaques sink inward; tactile structures
Component Tail Body Body*
develop between the organs, and some rows
Epithelial cells E E E of larval plaques are reduced or lost. At meta-
Surface keratinocytes E E E morphosis the innervation of the lateral line
Keratínized beak cells E —
Hatching gland cells
—
— E
is augmented by the appearance of a small
—
— myelinated inhibitory nerve, which possibly
Cement gland cells
— E
Ciliary cells E E E switches off the lateral-line organs while the
Mucous surface cells E E E frog is swimming.
Merkel cells E E E
Stiftchenzellen (anurans) E E E
Mitochondria-rich cells E Ec E Some specialized cells develop into adhesive glands
Flask cells E E ventral to the mouth in anuran embryos, and elongate.
Goblet cells (Xenopus) E E — bottle-shaped cells form hatching glands on the head of
Leydig cells (salamanders) E E — embryos; both of these kinds of cells degenerate shortíy
Melanophores D, E D, E D, E
after hatching. In anurans some epidermal cells are ker-
Xanthophores — D D
Iridophores D D D atinized to form the beaks and denudes of tadpoles; these
Mesenchymal macrophages D, E D, E D, E structures degenerate at metamorphic climax. Other epi-
Mesenchymal fibroblasts D D D dermal structures include immigrant melanophores, poly-
Granulocytes D, E D, E D, E morphonuclear neutrophils, granulocytes, mesenchymal
Polymorphonuclear leucocytes D,E D, E D, E
Nerve flbers D, E D, E D, E macrophages, and nerve flbers.
Schwann cells D D D During larval Ufe the dermis becomes organized and
Neuroblast organs E E Ed many structures appear by metamorphic climax. These
Striated muscle tissue D D D include melanophores, xanthophores, iridophores, gran-
Smooth muscle tissue D D D ulocytes and other leucocytes usually in capillaries, mes-
Mucous and granular glands — D D
enchymal fibroblasts and macrophages, and multicellular
"Adapted from Fox (1981). mucous and granular (serous) glands. These glands open
bE is Epidermis, D is dermis.
"Bladder (Bu/o) and palate (Rana). by means of ducts at the surface of the skin at climax.
dXenopus and oblígate neotenic salamanders. Also there are muscle fibers and nerve components, in-
 Metamorphosis
185

Figure 7-2. Adult and recently

metamorphosed young of
Ambystoma opacum from
Centreville, Virginia, showing
differences in color pattern. Photo by
K. Nemuras.

«iíding Schwann cells (nucleated neurosheaths) (Table able in those anurans that have thick, glandular skin as
7-3). adults (e.g., Bufo). Many recently metamorphosed am-
Thus, during larval development and metamorphosis phibians have color patterns unlike those of the adults
Ihe dermis is continually becoming more complex and (Fig. 7-2); the adult pattern usually develops within a few
approachmg the condiüon in adults, whereas the epider- days after the completion of morphological metamor-
mis undergoes various stages of appearance and disap- phosis. The striking blue and yellow bars on the flanks
pearance of cellular structures before assuming the adult of the hylid Agalychnis callidryas only become apparent
eondition. In general, cellular degeneration of larval ep- several weeks after metamorphosis, during which üme
idermis occurs by autolysis, demonstrated by autophagy the iris changes from gold to red (P. Starrett, 1960).
and the presence of cytolysosomes (Fox, 1981). Some
necrotic cells, such as those of hatching glands and ad- Musculature
hesive glands, probably are phagocytosed by neighbor- Head and body muscles present in larvae undergo re-
ing macrophages. Likewise, probably most of the rem- modeling during metamorphosis. In Rana pipiens expo-
nants of autolysed cells of the external gills suffer sure of the m. rectus abdominis to hormonal changes,
phagocytosis. Epidermal cells autolyze, keratinize, and which presumably are similar throughout the muscle, elicits
are shed. proliferation of fibers medially and degeneration of fibers
There is variable influence of thyroid hormones on the laterally (K. Lynch, 1984). This contrasts with the re-
origin, development, and subsequent degeneration of modeling of the jaw musculature during metamorphosis,
dermal and epidemial structures. The life cycles of ciliary which entails the loss of larval muscle fibers and their
cpfl$. and the cells comprising hatching glands, adhesive simultaneous replacement by new fibers that form the
<^ands, and epithelial gilí filaments probably are inde- adult muscles (Alley and Cameron, 1983).
pcndent of thyroid hormones, as are the origin and dif-
ferentiation of Stiftchenzellen, Merkel cells, chromato- Tail
phores, mitochondria-rich cells, neuromast cells, and Upon metamorphosis the caudal fins of salamander and
mesenchymal flbroblasts (Fox, 1981). The origin and dif- caecilian larvae are resorbed. Presumably the resorption
ferentiaüon of epidemial flask cells and skin glands and of the fins is accomplished in the same way as the de-
abo the ultímate loss of beaks and denudes in tadpoles generation of the entire tail in anuran tadpoles. In anu-
and keratínized lips in salamander larvae seem to depend rans the degeneration of the tail begins with the fins,
on a threshold level of thyroid hormone. followed by the distal musculature, and finally the prox-
The adult conditions of glandular development or pig- imal musculature. Resorption of tissues in salamanders
mentation are not necessarily attained at metamorphosis. terminales with the caudal fins, but the controlling factors
The development of dermal glands continúes after the that halt degeneration at that point are not known. As
froglet assumes a terrestrial life; this is partícularly notíce- summarized by M. Dodd and J. Dodd (1976), tail re-
LIFE HISTORY
186 sorption is a remarkable example of controlled cell death. are much the same as in adults; in fact, the most notice-
Presumably this is genetically programmed, and the able changes in the gastrointestinal tract in salamanders
proximate controlling agent is thyroxin. Autolysis and occurs just before the young larvae begin to feed. At that
phagocytosis are the main agents responsible for tail re- time the last of the yolk is absorbed, and peristalsis be-
sorpüon, but lysosomes may play a role. Caudal tissues gins. Subsequent changes in the gut involve the increase
become increasingly acidic during metamorphic climax, in the surface of the epithelial lining by folding and the
as various acid hydrolases accumulate in the üssues; these development of microvilli.
are the principal enzymes associated with üssue degen- Whereas a true pepsin-secreting stomach is present in
eration. Apparently just prior to the initiatíon of tail re- larval salamanders (Kunz, 1924) and presumably in cae-
sorpüon, there is a thyroxin-stimulated synthesis of hy- cilians, a true stomach is absent in anuran larvae. Instead,
drolytíc enzymes, possibly by macrophages. the presumptive stomach región of the gut usually is not
enlarged and has associated with it a manicorto gland in
Limbs most anuran larvae. The gland is absent in pelobatids
The growth of the limbs of all amphibians that have them and bufonids, and its occurrence is sporadic in some other
is a continuous process from early limb-bud stages with groups (Griffiths, 1961). The manicorto gland develops
no dramaüc changes during metamorphosis. The hind- in late embryonic stages and is formed from elements of
limbs of anuran larvae develop in much the same way the ventral pancreatic anlage, which proliferates within
as those of salamander larvae, but in late prometamor- the wall of the gut. In most tadpoles a connection be-
phosis certain structures, such as subarticular and meta- twáen the páncreas and the manicorto gland persists only
tarsal tubercles, toe pads, and webbing, develop. The until early premetamorphosis. Typically the manicorto
forelimbs of anurans that have aquatic larvae develop in gland surrounds the foregut; the gland consists of long
peribranchial sacs within the branchial chamber and cords arranged in a complex pattem of branching crypts
emerge well developed at the beginning of metamorphic that communicate with the lumen of the gut, not by de-
climax. The skin covering the developing forelimbs be- finitive ducts, but through irregular gaps in the epithe-
comes thin and transparent before the eruption of the lium. In most kinds of tadpoles, the lumen of the foregut
limbs. In at least some frogs having direct development in the región of the manicorto gland is lined with ciliated
(e.g., Eleutherodactylus), the forelimbs develop exter- epithelium enclosed in a sheath of circular muscle. There
nally. Subsequent to metamorphosis, tubercles and other are some notable deviations from the typical develop-
structures, such as toe pads, continué to differentiate and ment and structure. Tadpoles of Xenopus, Rana macro-
develop into the adult form. Webbing between the toes dacfyla, and Heleophryne rosei retain a connection be-
of recently metamorphosed frogs commonly is much less tween the páncreas and the manicorto gland until
extensive than in adults. Limb growth and development metamorphosis. Camivorous tadpoles of Ceratophiys and
are dependent on thyroxin, as is the eruption of the fore- Occidozyga have a thick muscular coat surrounding the
limbs in anurans. gland, no cilia in the lumen of the foregut, and a greatiy
reduced number of epithelial perforations. In microhylid
Alimentan; Canal tadpoles the pattern of the crypts is more complex, and
The gross structure of the alimentan; canal does not change the crypts are more extensive than those of other tad-
much during metamorphosis in salamanders and caeci- poles. The manicorto gland is limited to the pancreatic
lians, although the small intestine in at least one sala- side of the gut in Alytes obstetrícans, but the gland en-
mander, Ambystoma tigrinum, is about 25% shorter in circles the foregut in other discoglossids that have been
adults than in larvae (Tilley, 1964). However, in anuran studied. In the tadpoles of the rhacophorid Philautus gryl-
tadpoles the digestive tract consists mainly of a long, coiled lus the manicorto gland is modified into a muscular diver-
intestine, which undergoes drastic changes at metamor- ticulum connected to the lumen of the foregut by two
phosis. Other changes also occur. ciliated cañáis and another opening that permits only dis-
The epithelium in the buccal cavity retains the goblet charge into the foregut. These various modificaüons might
cells present in larvae, but other structures develop de be correlated with the dietary habits of the tadpoles (Grif-
novo, including: (1) intermaxillary glands posterior to the fiths, 1961).
premaxillae and between the nasal capsules; (2) palatine The postesophageal part of the foregut that is associ-
glands associated with the prevomerine teeth; (3) cilia, ated with the manicorto gland apparently has no digestive
which are especially numerous and active in the vicinity functions and serves only for the storage of food. During
of the outlets of the intermaxillary glands; and (4) a tongue metamorphosis the cells of the manicorto gland degen-
derived from muscle tissue in the floor of the mouth. In erate and are replaced by new cells incorporated into the
salamanders, and presumably in caecilians, the adult gut; the new cells secrete pepsin, so it is at this time that
tongue incorpora tes a "primary" tongue that develops in a functional stomach is formed. The midgut or intestine
larvae, whereas the tongue in anurans is a completely shrinks greatiy; the luminal cilia are replaced by microvillL
new structure. The major changes in the alimentary canal begin prior to
The digestive tracts of salamander and caecilian larvae the emergence of the forelimbs. During this dramatic shift
 Metamorphosis
the digestíve system to change from the digestión of - pronephros 187
particles of plant material to large pieces of animal
issues, the metamorphosing froglet is incapáble of di-
§esting any kind of food for several days.

Páncreas
h late prometamorphosis, the exocrine páncreas begins
to dccrease in size; this seems to be caused in part by
fee degeneration of acinar cells and tissues and also by
ijehydration. Degeneration occurs by autolysis, but prob-
dbK some phagocytosis ensues. Absolute reduction in
wkime of the páncreas may be as much as 80%. Im-
•ediately after metamorphosis the páncreas increases in
aze. with a relatively larger increase in the endocrine
fesue because of proliferating islets of specialized types
tí cells. New RNA is synthesized as the páncreas regen-
erares; perhaps some predetermined cells need to de-
generate in order to permit the remaining rudimentary
páncreas to develop into the adult páncreas (Fox, 1981).
These changes in the páncreas are induced by thyroxin.

Urogenital System
Larval amphibians have a relatively primitive type of kid-
•ey that functions primarily in the excretion of water and
anamonia, whereas in terrestrial adults the kidney func-
to conserve water and excrete urea. Concomitant
the morphological metamorphosis of the kidney is
f*e development and differentiation of the gonads (Fig.
7-3).
The larval kidney is the pronephros which forms from
*»e anterior nephrostomes and persists throughout larval
He only to regress and disappear by the end of meta-
morphosis in salamanders and anurans. Degeneration starts
a: about the time of the onset of metamorphic climax
and is complete by the end of metamorphosis. Degen-
eration involves autolysis and phagocytosis; lysosomes in
tbe form of degeneration bodies also may be important.
Pronephric growth, differentiation, and ultímate degen- Figure 7-3. Diagrammatic representaron of the development of
the urogenital system in anurans. A. Young larva with three
eration are controlled mainly by circulating thyroid hor- nephrostomes, Wolffian ducts, and germinal ridges. B. Late larva
nones. Structurally the pronephros is a tightly arranged with functional pronephros and mesonephros. C. Metamorphosis
•tass of tubules with ciliated nephrostomial ducts leading with degeneration of pronephros and anterior part of the Wolffian
duct. D. Undifferentiated state of genital tract. E. Sexually
to the coelom. Anurans have three nephrostomial ducts; differentiated male. F. Sexually differentiated témale. Gonads are
primitive salamanders (cryptobranchids) have five, and shaded. Based on Gallien (1958).
more advanced salamanders, only two. Caecilians, in
which the pronephros is greatly elongate, have 8 to 12
nephrostomial ducts. The nephrostomial tubules join to in salamanders, whereas only the posterior nephrostomal
form a common rubule, the Wolffian duct. Evaginations tissues persist in anurans. In these mesonephric kidneys,
of the dorsal aorta form paired glomeruli, which are par- along with the opisthonephric kidneys of caecilians, the
fiaDy surrounded by outpocketings of the nephrostomial tubular connections with the coelom have been lost, and
(kicts (Bowman's capsules). the glomeruli are contained within Bowman's capsules.
In caecilians the anterior part of the kidney remains Genital ridges are formed by sexually Undifferentiated
intact and, together with differentíating nephric tissue from primordia in the peritoneal cavity in cióse association with
the middle and posterior nephrostomes, persists in adults the nephrostomes. Parts of these ridges give rise to the
as an elongate opisthonephros connected by tubules to gonads; the anterior parís form the fat bodies (Franchi et
the Wolffian duct throughout its entire length. Prior to al, 1962). The genital ridges develop in a posterior di-
the degeneration of the pronephros, the middle and pos- rection, and two áreas become distinct—a peripheral cor-
terior nephrostomes differentiate into functional kidneys tex derived from proliferation of the peritoneal epithe-
LIFE HISTORY
188 l¡um; an¿ an ¡nner medulla. Concomitant with the been demonstrated to be effected directly by increased
development of the genital ridges, primordial germ cells, amounts of thyroid hormone (T4). However, many neural
which origínate from extragonadal sources, migrate into structures have yet to be studied with respect to modifi-
the ridges by passive movements induced by differential cations that occur during development, particularly dur-
growth of the embryonic üssues. In anurans the germ ing or near metamorphic climax.
cells are derived from presumptive endoderm, but trióse Gross changes in the central nervous system, which is
in salamanders are thought to origínate from lateral-plate well developed by prometamorphosis, include (in anu-
mesoderm (Franchi et al, 1962). The origin of germ cells rans) reduction in size but thickening of the walls of the
in caecilians is unknown. Later differentiaüon of the go- ventricles of the cerebellum and medulla oblongata,
nads follows different patterns in males and females. Pro- widening and shortening of the diencephalon, and nar-
liferation of the cortex with a concomitant regression of rowing and shortening of the fossa rhomboidalis of the
the medulla forms hollow ovaries by folding of the ger- medulla. In tadpoles the cerebellum remains in a rela-
minal ridge; the interna! lining of the ovaries is medullary tively early developmental stage during premetamor-
in origin. The reverse is true in males; the medulla de- phosis, and has a more rapid development during
velops into testes, while the cortex regresses. In the un- prometamorphosis and a rapid maturation during meta-
differenüated gonads, mesenchyme cells sepárate the morphic climax. Some of the changes are associated with
medullary tissue from the cortex; these cells eventually corresponding modifications of the shape of the chon-
give rise to the tunic ensheathing the testes. In the Bu- drocranium as it ossifies. By comparison, changes in the
fonidae, cortical remnants of the germinal ridge form Bid- gross morphology of the brains in salamanders are slight.
der's organs in males. These round structures on the The spinal cord differenüates proximodistally and en-
anterior ends of the testes consist of a compact mass of ters the tail in early premetamorphosis, and incipient dor-
small oocytes surrounding a vestigial ovarían cavity; these sal root ganglia are evident at that time. During meta-
oocytes remain in an immature state. morphic climax there is selectivo degeneration of some
During development two pairs of ducts are derived cellular components of the spinal cord and ganglia in the
from primitíve kidney ducts and develop in both sexes body, whereas there is complete degeneration of those
to become the forerunners of the adult genital ducts. in the tail of anurans.
These are the Müllerian and Wolffian ducts; each pair Studies on some special cells in the nervous system
extends from the primordial gonads to the cloaca. Com- have revealed notable modifications during metamorphic
monly both sets of ducts are present in larvae; upon climax. Paired Mauthner cells, on each side of the me-
metamorphosis the Müllerian ducts tend to degenerate dulla, have long axons extending through the trunk cord
in males, whereas in females they become the functional to the tail. These cells are considered to be adaptations
oviducts. The Wolffian ducts persist in both sexes. In to aquatíc life and disappear in anurans at or shortly after
larval amphibians the Wolffian ducts first function as the metamorphic climax. They persist for as long as 2 months
primary nephric ducts draining the pronephric tubules, after metamorphosis in Xenopus and are unknown in
and later they become the mesonephric ducts. In females Bu/o (Moulton et al., 1968). The development and growth
the Wolffian ducts retain their exclusively excretory func- of the Mauthner cells is controlled by increasing levéis of
tion, but in males they also serve as genital ducts after circulatíng thyroid hormones in pre- and postmetamor-
the efferent ductules of the medullary cords join the phosis, and their disappearance seems to be associated
mesonephric tubules. Unlike the Müllerian ducts, the with the dramatic decrease in circulating thyroid hor-
Wolffian ducts retain no connection with the nephric tu- mones at metamorphic climax.
bules. There is variable regression of the Müllerian ducts Rohon-Beard cells are primary sensory cells located
in male anurans; usually they regress to small rudiments, on either side of the dorsal midline of the spinal cord in
but in some members of the Rana pipiens complex they tadpoles. They develop anteroposteriorly in the body and
persist throughout Ufe as complete ducts. then the tail. They are present in maximal numbers in
The gonads and their producís differentíate and de- early premetamorphosis. Thereafter, cell loss proceeds
velop continuously during larval life in caecilians and sal- gradually anteroposteriorly, and by late prometamor-
amanders, whereas in anurans the testes may differen- phosis only a few degenerating cells remain. Degenera-
tíate and mature well before metamorphic climax (e.g., tion of Rohon-Beard cells occurs earlier in Xenopus trian
Pleurodema cinérea), shortly before metamorphic climax in Rana (Nieuwkoop and Faber, 1976). Because cell loss
(e.g., Ceratophrys ornata and Rana catesbeianaj, or long occurs so early in larval life, it is unlikely that the loss is
after metamorphosis (e.g., Bufo arenarum) (Lofts, 1974). related directly to thyroid hormones; more likely the loss
In anurans the ovaries do not mature untíl well after is related to the early development of the spinal ganglia,
metamorphosis. which take over the sensory functions initially assumed
by the Rohon-Beard cells (Kollros, 1981). However, final
Nervous System degeneration at metamorphic climax may be influenced
The general transitions in the nervous system during by changing levéis of thyroid hormones (Stephens, 1965).
metamorphosis have been summarized by Kollros (1981) The cells of the lateral motor column provide motor
and Fox (1984). Changes in the nervous system have innervation to the limbs. The development of the lumbar
 Metamorphosis
i occurs in late embryonic stages, and the brachial epidemial folds. Also, at metamorphic climax the tendón 189
í ir prometamorphosis. The number of cells increases of the nictítating membrane and the lacrimal duct de-
i máximum and then declines gradually to metamor- velop. These structures do not develop, or develop only
: dmax, when the number stabilizes. Thyroid hor- parüally, in oblígate neotenic salamanders and pipid frogs.
i are essential for the growth and differentiation of In caecilians the eyes degenerate and are covered by a
ífcteral motor column neurons, but increased levéis thin layer of bone and/or skin.
ating thyroid hormones in late prometamorphosis Changes in the optical propertíes of the eyes of Sala-
ntiy stabilize the number of cells. mandra salamandra and Pelobates syriacus were docu-
maturatíon changes in the cerebellum include a mented by Sivak and Warburg (1980, 1983), who found
in the number of external granule cells, the that during metamorphosis there is change from a spher-
i of most of these cells into the internal granular ical lens to a flattened lens. This change is much more
and the conversión of small, immature Purkinje gradual in Pelobates than in Salamandra; in fací, the
irte large, mature ones. Purkinje cells are flask-shaped refractory power of the lenses of tadpoles ¡n late pro-
í forming an incomplete layer between the molecular metamorphosis is poor in the aquatic environment.
! nuclear layers of the cerebellar cortex. The growth Moreover, the alignment of the eyes changes from a lat-
1 maturatíon of the Purkinje cells is dependent on thy- eral plañe to an anterolateral plañe; this takes place dur-
I hormones. ing metamorphic climax at the tíme of the development
Ibe proprioceptors of the jaw musculature, the cells of of the sclerotíc ring that supports the eye in metamor-
i mesencephalic nucleus of the trigémina! nerve, ap- phosed amphibians.
• in the optíc tectum just as feeding begins in larval Eyes are poorly developed in subterranean salaman-
ama and Rana. The number of cells increases ders. In Proteus, Haideotriton, and Typh/omo/ge, lenses
' during development, and in Rana the number of and retínal structures fail to develop completely, and in
& is highest just prior to metamorphic climax; this sug- juveniles the vestíges of these structures degenerate.
E that some cells die during climax. In Ambystoma However, in Typhlotriton the eye structures develop fully,
sze of the cells decreases with time, but in Rana the but in juveniles there is partial degeneratíon (Besharse
; remains small throughout most of the larval period, and Branden, 1974).
: to increase in prometamorphosis, increases more The chemosensory organs of Jacobson develop as
during metamorphic climax, and increases more ventromedian grooves in the floor of the nasal sacs. With
after metamorphosis. The observed differences the exceptíon of Siren (Jurgens, 1971), the nasal sacs
tefeseen Rana and Ambystoma may be related to the rotate on their longitudinal axes so that the organs of
•uüficatíons of the suspensorium and associated mus- Jacobson lie in a lateral positíon. During metamorphic
eaferure in anurans, whereas few changes occur in these climax, the epithelial lining differentíates into the glands
jfcjctures in salamanders. The mesencephalic nucleus composing the organs.
•rife are insensitive to thyroid hormones at the tíme of During late prometamorphosis and metamorphic cli-
tfber appearance and also again several months after max, the nasolacrimal duct is formed from rodlike thick-
«esamorphosis; in the meantíme, sensitivity to thyroid enings of epidermal cells. According to Schmalhausen
tomones begins early in larval life and increases rapidly (1968), the duct has two origins—partly from the pos-
faough metamorphosis. terior nostril and partly from tíssues that gave rise to the
infraorbital seismosensory canal of crossopterygian fishes.
Sensory Structures At about the same tíme in development, orbital (or Har-
Most sensory structures undergo changes during meta- derian) glands develop as thickenings of epidermal cells
•crphosis; changes in the lateral-line system are dis- immediately anterior to the eye.
OEsed in the section Integument, and the development In caecilians, the tentacle develops in late embryos and
at the ear is discussed in the section Skeleton. is evident in young free-swimming larvae. The tentacular
In larval amphibians, internal and external corneas are sheath probably represents the enlarged common duct
separated by intraorbital fluid. These cornea fuse at of the orbital glands, which in caecilians functíon to lu-
«etamorphic climax to form the single adult cornea. In brícate the tentacular sheath rather than the degenerate
fate premetamorphosis and during metamorphic climax eyes. The tentacle develops from a longitudinal epithelial
ihe relaüvely thin and weakly developed extrinsic ocular fold in the wall of the duct (Badenhorst, 1978). The re-
muscles grow enormously and simultaneously shift their tractor muscle of the tentacle is homologous with the m.
points of origin mediad on the parasphenoid. The eye retractor bulbi of anurans and salamanders.
teelf increases in size, and this growth, in combination
with the growth of the extrinsic ocular muscles, produces
the bulging eyes characteristíc of most amphibians (ex- NEOTENY
cept caecilians and oblígate neotenic salamanders). Dur- The phenomenon of attaining reproductíve maturity while
ing metamorphic climax in most salamanders and anu- retaining the larval external morphology has been known
rans, accessory structures—upper and lower eyelids, in salamanders since the middle of the last century. The
-:ctitating membrane, and conjunctíval sacs—develop from multiplicity of terminology referencing aspects of delayed
LIFE HISTORY
190 somatic maturity and precocious reproductiva maturity who summarized the evidence that larval reproducüon in
has hampered effective communication. Well-entrenched salamanders is the result of delayed somatic development
terms such as neoteny, paedogenesis, and paedomor- and not precocious reproductive development. Thus, it
phosis have been variously redefined (e.g., Pierce and seems that paedogenesis is not a common cause of larval
H. Smith, 1979); new terms such as progenesis (S. Gould, reproductíon in salamanders, and the general phenom-
1977) and parthenopaedogenesis (Dubois, 1979b) have enon of reproductíon by salamanders in their larval state
been introduced. may be justífiably termed neoteny in both the broad and
Neoteny is used here in the sense of Gould (1977), narrow sense of the term. Paedogenesis should be ap-

Table 7-4. Taxonomic Occurrence of Neoteny in Salamanders

Taxon Referente
Hynobiidae
Hynobius lichenatus Sasaki (1924)
Cryptobranchidae
Crypíobranchus af/eganiensis* Nickerson and Mays (1973)
Andrias
davidianus* Liu (1950)
japonicus* Stejneger (1907)
Sirenidae
Pseudobranchus stríatus* Martof (1974)
Siren (2 species)* Martof (1974)
Salamandridae
Notophthalmus
perstriatus Bishop (1943)
uiridescens Branden and Bremer (1966)
Triturus
alpestris Rocek (1974)
cristatus Dely (1967)
helveticus Gabrion et al. (1977)
Amphiumidae
Amphiuma (3 species)* Salthe (1973)
Proteidae
Necturus (5 species)* Hecht (1958)
Proteus anguinus* Briegleb (1962a)
Ambystomatídae
Ambystoma
dumeriln* Branden (1970a)
gracile Sprules (1974b)
lacustris* Tihen (1969)
lemaense* Tihen (1969)
mexicanum* Brunst (1955)
ordinarium J. Anderson and Worthington (1971)
subsa/sum* Tihen (1969)
talpoideum A. F. Carr and C. Goin (1943)
tigrinum Gehlbach (1967)
Rhyacosiredon altamirani Brandon and Alüg (1973)
Dicamptodontídae
Dicamptodon ensatas Nussbaum (1976)
Plethodonüdae
Eurycea
íatiíans* B. Brown (1967a)
multiplícate Dundee (1965a)
nana* B. Brown (1967b)
neotenes Sweet (1977a)
tridentífera* Sweet (1977b)
troglodytes* J. Baker (1966)
tynerensis* Dundee (1965b)
Gyrinophilus palleucus* Brandon (1966a)
Haideotriton wallacei* Brandon (1967b)
Typhlomolge
rathbuni* Porter and Sweet (1981)
robusta* Potter and Sweet (1981)
Typhlotriton spe/aeus Brandon (1970b)
"Oblígate neotenes in nature.
 Metamorphosis
••Ue 7-5. Comparative Pattems of Metamorphosis in Genera of Oblígate Neotenic Families of Salamanders 191
Cerato- Septo- Gilí
Genos branchials MaxiUae maxlUae Lacrimáis Gills slits Skin
l'Jtaüos 2 + - - 0 0 Adult
| &sptobranchus 4 + - - 0 1 Adult
i Reudobranchus 4 + + + 1 1 Larval
!&en 4 + + + 3 3 Adult
; Jfadurus 3 + + 3 2 Larval
tltaeus 3 — + + 3 2 Larval
4 + + + 0 1 Adult

peed only when direct evidence suggests that larvae are it was referenced in 3311 books and articles from 1615
í «acually mature as the result of accelerated reproducüve to 1970 (H. Smith and R. B. Smith, 1971). Much of this
i áevelopment. literature has dealt with experimental embryology and
endocrinology of laboratory-reared animáis in the United
i Occurrence of Neoteny States and Europe. The largest of the neotenic Ambys-
[i MI members of four families of Salamanders are neotenic, toma is A. dumeri/ii (Fig. 7-4).
•d at least some populatíons of Salamanders in all other Spontaneous metamorphosis has been reported for
I Bcmlies have neotenic individuáis (Table 7-4). Aquatic Ambystoma dumeriffi and A. mexicanum (Branden, 1976;
•rvae are highly transitory in caecilians, and it is most H. Smith and R. B. Smith, 1971), but in each case the
«dkely that any are neotenic. Although "neotenic" anu- animáis were stressed during shipment or manipulation
1 an larvae have been described from time to time, these in the laboratory, or they survived for only short periods
' aÉ have been individuáis with abnormal thyroid glands of time. There are no substantiated reporta of either of
' nal resulted in failure to metamorphose completely, and these species undergoing metamorphosis in their natural
i Bese fail to reproduce (Wassersug, 1975). Space for the habitat. Four species of Ambystoma are facultatively neo-
jpjnads and especially for the storage of eggs does not tenic; some populations norrnally metamorphose, whereas
tocóme available until metamorphosis of anuran larvae. others do not unless their aquatic environment becomes
The fifteen species of oblígate neotenic Salamanders uninhabitable. The best known of these facultative Am-
«onstituting all of the living species of four families exhibit bystoma are A. gracile and A. íigrinum (Fig. 7-5). Like-
Bfierent patterns of partial metamorphosis (Table 7-5). wise, one Hynobius and five newts have populations that
These range from the failure of certain cranial and jaw sometimes do not metamorphose, whereas other popu-
dtements to develop to the retention of larval skin con- lations do metamorphose into terrestrial adults. Only three
atning Leydig cells. Salamanders of the genera Andrias, of twelve neotenic species of hemidactyline plethodontids
Cryptobranchus, and Amphiuma resorb their gills, and are known to metamorphose in nature. The most spe-
in Andrias the gilí slits cióse. Three pairs of external gills cialized of the oblígate neotenes among the plethodontids
are retained in adults of all of the others, except Pseu- are Haideotríton wallacei and the two species of Ty-
éobmnchus, which retains only one pair. phhmolge (Fig. 7-6).
Five species of Ambystoma and nine species of hemi-
dactyline plethodonüds are oblígate neotenes in nature, Endocrine Aspects of Neoteny
whereas fifteen species in four families are known to be The discovery of neotenic Salamanders provided exper-
facultatively neotenic. The most famous neotenic sala- imental biologists with ideal laboratory animáis for de-
mander is the Mexican axolotl, A. mexicanum (Fig. 7-4); termining the endocrinological control of metamorphosis;

Figure 7-4. Two neotenic species of

Ambystoma. (Left) A. mexicanum
from Lago Texcoco, México. (Right)
A. dumerilii from Lago de Pátzcuaro,
México. Both of these species are
confined to lakes on the southern
part of the Mexican Plateau and
norrnally do not metamorphose in
nature. Photos by H. B. Shaffer.
LIFE HISTORY
192

Figure 7-5. A neotenic,

subterranean plethodontid
salamander, Typhlomolge rathbuni,
(rom Ezell's Cave, Texas. The eyes
are degenerate, and the skin lacks
pigment. Photo by E. J. Maruska.

most of the knowledge is based on two species— Am- hypothalamic level (e.g., D. Morris and Platt, 1973; Tau-
bystoma mexicanum and A. figrinum. However, exper- rog et al., 1974). Whether externa! or interna! cues, which
imental work also has involved some of the neotenic actívate the axis, are lacking, or whether, for genetíc or
plethodontíds, as well as other species of Ambystoma. some other reasons, some individuáis are insensitíve to
In oblígate neotenes, such as Necturus, Proteus, and them is not known for certain. However, natural selectíon
Amphiuma, the major cause for cessation of metamor- may be operatíng to select genotypes for neoteny in áreas
phosis seems to be insensitivity of tissues to thyroid hor- of harsh terrestrial environments.
mone (J. Harris, 1956); treatment of these salamanders
with thyroid hormone may result in some initíal changes,
such as sloughing of skin or reduction of gills, but pro- ECOLOGICAL AND EVOLUTIONARY
longed treatment is lethal. Some neotenic plethodontíds SIGNIFICANCE OF METAMORPHOSIS
(Haideotriton and Typhlomolge) undergo partial meta- Theoretically, the ranges of body sizes at metamorphosis
morphosis when treated with thyroxin (Dundee, 1957, and the duratíon of the larval stage (and therefore tíme
1961), whereas others (Eurycea tynerensis and Gyríno- of metamorphosis) of individuáis in a given populatíon
philus palleucus) can be induced to complete metamor- are determined by a minimum body size that must be
phosis (Kezer, 1952; Dent and Kirby-Smith, 1963). attained and a máximum body size that cannot be ex-
Experiments with facultatívely neotenic Ambystoma ceeded at metamorphosis (Wilbur and Collins, 1973).
have demonstrated that thyroid hormone (T4) readily in- Between these two size thresholds, the endocrinological
duces metamorphosis and that the thyroids of these sal- initiatíon of metamorphosis is expected to be related to
amanders are sensitive to thyroid-stimulaüng hormone the recent growth history of the individual larva. Species
(Taurog, 1974). Similar results were obtained from ex- that exploit ephemeral aquatic environments, such as
periments on newts—Notophthalmus viridescens (Dent, temporary ponds, will have a wide range of possible sizes
1968) and Triturus helvéticas (Gabrion and Sentein, 1972). at metamorphosis, whereas those developing in relatívely
There is a low rate of uptake of labeled iodine by the stable environments will have a narrow range.
thyroids of neotenic salamanders; the rates of facultative According to Wilbur and Collins' (1973) interpretatíon
neotenes is intermedíate between the rates of oblígate of their extensive observations and experiments on Am-
neotenes and those of species that normally metamor- bystoma maculatum and Rana sylvatica, the large vari-
phose (D. Morris and Platt, 1974). ation in the length of the larval period and body size ai
Nearly all of the evidence indicates that in facultatively metamorphosis cannot be explained solely by differences
neotenic salamanders the level of activity in the hypo- in dates of hatching or egg sizes. Therefore, they pro-
thalamo-pituitary-thyroid axis is very low, and most re- posed that as development proceeds, variation in expo-
sults support the view that the primary failure is at the nenttal growth coefficients causes a trend from a normal
 Metamorphosis
| K a skewed distribuüon of body sizes. The degree of the animal is unable to feed. By this time, larval growth 193
wing increases, and the median of the distribution has ceased, and all nutrition is provided by the resorption
|jfcnreases, with increasing iniüal densiües of populaüons. of the tail. Moreover, the period of transformation from
! relative advantages of the largest members of a co- a tadpole that propels itself through water by means of
: may arise from a variety of mechanisms including its tail to a frog that propels itself through air by means
producirán of growth inhibitors, interference com- of jumping is a critical period in the survivorship of the
and size-selectíve feeding behavior. These animal. It has been demonstrated experimentally (in
lisms result in a nonnormal distribution of com- Pseudacris triseríata) that metamorphosing tadpoles can-
ability, a possible source of the density-de- not sustain swimming nearly as effectively as tadpoles
ent competition coefficient found in many species that do not have visible forelimbs; furthermore, froglets
¡fWfcur, 1972). that still have a tail are ineffective hoppers as compared
As noted by Wilbur and Collins (1973), teleologially with those that have resorbed their tails completely (Was-
be decisión to initiate metamorphosis is an educated sersug and Sperry, 1977). Analysis of stomach contents
| fcdaptive) guess that the risk of metamorphosis is less of garter snakes (Thamnopfiis) reveáis that these snakes
i the risk of remaining in the aquatic habitat. Lack of are most effective preying on metamorphic stages of sev-
| faod and/or desiccation of the aquatic habitat are two eral species of anurans (Wassersug and Sperry, 1977;
or factors that may "forcé" larvae to metamorphose, Arnold and Wassersug, 1978). Vulnerability to predation
' í íhey have reached the critical minimum size and nec- is an ecological obstacle that can be minimized by
r esary hormonal levéis. Because the larval stage is a pe- undergoing metamorphosis rapidly and by synchrony of
•oc of intense feeding and rapid growth, early meta- metamorphosis in cohorts of tadpoles.
•orphosis may result in small, malnourished young that The occurrence of either facultative or oblígate neo-
have low survivorship, and those that do survive may teny among species in the Hynobiidae, Salamandridae,
| nequire moretimeto reach reproductive maturity than Ambystomatidae, and Plethodontidae is primarily re-
tfeose that metamorphose at larger sizes. stricted to populations inhabiting permanent aquatic hab-
However, availability of food and stability of the aquatic itats in high montane or arid environments, and usually
iabitat are not the only factors that may be responsible where fishes are rare or absent. Thus, neotenic popula-
fcr the initiation of metamorphosis. In high-elevation tions of Hynobius lichenatus and populations of various
populations of Ambystoma tigrinum in the Rocky Moun- species of Triturus and Ambystoma are neotenic in such
teins. temperature of the aquatic habitat determines the habitáis, whereas at lower elevations or in more mesic
SZE at, and time of, metamorphosis (Bizer, 1978). Growth habitats populations of the same species characteristically
Bles of larvae increase at higher temperatures, whereas metamorphose.
szes of larvae at metamorphosis decrease at higher tem- With respect to Ambystoma, Sprules (1974a) sum-
peratures. Thus, there is a negative correlation between marized evidence on the occurrence of neoteny in per-
yowth rate and size at metamorphosis in these high- manent aquatic situations. In regions where there exist
devation populations. harsh terrestrial conditions, such as severe temperature
Temperature-dependent rates of development have fluctuations, lack of suitable cover or food, and low hu-
been established for various species of amphibians midity, neoteny will evolve because salamanders that spend
(Chapter 5), but although endocrine production also is their entire lives in the larval form in the water have an
correlated with temperature in amphibian larvae, the rates adaptive advantage over those that metamorphose and
of production and circulation of hormones and the de- become primarily terrestrial. These conclusions specifi-
yee of sensitivity of target tissues to the hormones with cally apply to several species of Ambystoma and Triturus.
respect to temperature remain essentially unknown. The facultative response to environmental conditions
Therefore, the proposed minimum size at metamorphosis provides an intraspecific flexibility that certainly is adap-
is only one facet of the developmental problems that tively advantageous over being locked into either oblígate
must be overeóme before metamorphosis can be com- neoteny or normal metamorphosis.
pleted successfully. The endocrinological aspects of There is a high correlation between the presence of
metamorphosis need to be studied under diverse envi- facultatively neotenic Ambystoma and Notophthalmus and
ronmental conditions to arrive at an understanding of the absence of fishes (Sprules, 1974a; Petranka, 1983);
possible synergistic effects of hormones and environ- yet the oblígate neotene A. dumeri/ü coexists with nu-
mental factors (temperature, light, crowding), as well as merous species of fishes in Lake Pátzcuaro in México.
nutritional state. Perhaps coexistence is possible because of the large size
The transition from larvae to terrestrial adults in sala- of the salamanders and/or their nocturnal habits.
manders is a gradual change during which the animáis Populations of neotenic Triturus in Europe have not
are feeding continuously and seem to have no period of been studied as thoroughly as Ambystoma in North
locomotor inhibition. In contrast, metamorphosis in anu- America, but in each species neoteny occurs in popula-
rans involves a period of degeneration of larval mouth- tions living in permanent water in harsh terrestrial envi-
parts and development of adult jaws, during which time ronments. On limestone plateaus in southern France, the
LIFE HISTORY
194 ponds inhabited by T. helveticus have no iodine defi- this situatíon neotenic individuáis can feed while they are
ciency; furthermore, there is a significan! positive corre- underground, but adaptatíons for terrestrial feeding in
latíon between the frequency of neoteny and the con- metamorphosed individuáis are ineffecüve underwater and
centraüons of calcium, magnesium, and phosphorus in darkness.
(Gabrion et al., 1978). The importance of these ions to On the basis of the foregoing ideas regarding the adap-
the maintenance of neoteny, if any, is unknown. tive significance of facultative neoteny, it is tempüng to
Neoteny in hemidactyline plethodontids is associated hypothesize that all cases of neoteny in salamanders
with subterranean species living in limestone regions. Those evolved in response to unfavorable terrestrial environ-
species that are restricted to deep subterranean waters ments. Permanence and stability of aquatic habitats, such
are oblígate neotenes, whereas those species that inhabit as subterranean streams and rivers in ancient positive
surface waters, as well as subterranean waters, com- land masses, could result in salamanders that live in those
monly are facultatively neotenic. Thus, Haideotriton and habitats losing the ability to metamorphose through the
Typh/omo/ge are examples of the oblígate extreme, and insensitivity of üssues to thyroid hormone. Thus, oblígate
Eurycea neotenes and Typhlotriton spelaeus are facul- neotenes, such as proteids, sirenids, and amphiumids,
tative neotenes intermedíate ecologically between the may have become neotenic in response to unfavorable
oblígate neotenes and those species of Eurycea that terrestrial environments in the Cretaceous, whereas the
undergo normal metamorphosis in surface waters. The neotenic plethodontids may have adapted to subterra-
origin of neoteny in Eurycea on the Edwards Plateau in nean aquatic habitats at the time of the developing grass-
central Texas is related to the limitaüon of suitable habitat lands in the Miocene. The distribution and generally fac-
(Sweet, 1977a). During periods of drought when the dis- ultative neoteny of newts and Ambystoma suggest that
charge of surface springs diminishes, salamanders must neoteny in these salamanders may be more recent, pos-
retreat underground via spring channels. The selective sibly adaptive responses to Pleistocene and Recent cli-
disadvantages of metamorphosis may be most pro- matic changes.
nounced under conditíons of unreliable spring flow; in
PART

ECOLOGY
 CHAPTER 8
-T, the poorfrog, his behavioral and
rr.sio/ogi'ca/ problems are so complicated
ir 2 mterrelated, it is amazing that we can
j-.derstancí them and he is ulive at all!
Bayard H. Brattstrom (1979)
Relationships
with the
Eiiviro ii me ni

A kmphibians, especially those that have lefl the water,

aer.erally inhábil environments that are hostile to their
Allhough for purposes of organizalion Ihe material in
Ihis chapter is discussed under specific headings of water
rase physiology. Because they are ectotherms and have economy, lemperalure, ele., il musí be kepl in mind Ihal
i permeable body covering, they are more susceptible Ihe mechanisms involved in one aspecl of the organism's
D the vicissitudes of the environment than any other physiology cannof be dissocialed enlirely from anolher.
•Kiapods. Nevertheless, by combinations of many unique The physiological inleraclion of amphibians wilh Iheir
—.crphological structures, physiological mechanisms, and abiolic environmenl is a complex, dynamic syslem of
rtr.avioral responses, they have adapted to life in nearly related processes.
al rerrestrial habitáis, ranging from Arctic lundra lo some
rr the driesl deserts in Ihe world, and from elevations of
—ore Ihan 5000 m lo sea level, even lo brackish man- WATER ECONOMY
arove swamps. However, when Ihe diversily of amphib- Aquatic species are bathed conslanlly by water; Ihus Ihey
2.-.S is examined, physiological limilations are apparenl, encounler no difficullies with water loss. However, ler-
recause the majority of species inhábil regions having reslrial amphibians have had lo evolve adaplations to
rsgh ambienl moislure and modérale lo warm lemper- cope with Ihe inevilable loss of body water while main-
iT-ires. laining a moisl skin for gas exchange. Their success is
Because of Iheir abundance and physiological char- exemplified besl in Ihe capabilily of some amphibians lo
acteristics, some amphibians, especially frogs of the ge- inhábil demanding, inhospitable deserts, where life poses
-_s ñaña and salamanders of Ihe genera Ambystoma, lwo major physiological problems—scarcily of water and
Trrurus, Sa/amandra, and Necturus, have been favorite environmenlal conditions thal accenluale water loss by
^xperimenlal animáis for laboralory physiologists for many evaporalion.
iecades. This chapter deals wilh the environmenlal phys- Water generally makes up 70-80% of Ihe body mass
«Díogy of amphibians. The major purpose of Ihe material of amphibians; Ihe higher percenlages are for aqualic
presenled herein is a synlhesis of Ihe ways amphibians species (Thorson, 1964). Water is exchanged readily wilh
exist wilh résped lo their abiolic environment Terreslrial Ihe environmenl, and water conserving mechanisms could
ronditions are emphasized, for most of Ihe physiological funclion polenlially al several sites:
problems associated wilh Ihe aqualic environment were
áscussed in relalion lo Ihe physiology of larvae in Chap- 1. Wherever oxidation lakes place Ihroughoul Ihe
body, melabolic water is produced. This is
197
ECOLOGY
198 added lo the watery médium of the proto- solalion and air cúrrente. Thus, Ihe undersides of slones,
plasm and is subject to loss from the body inleriors of logs, depths of leaf mulch, shaded crevices,
only, indirectly, as is water from other sources. and axils of leaves of aroids and bromeliads, as well as
However, producüon of metabolic water burrows in Ihe soil, are common diurnal shellers for ter-
amounts to less than 0.01% of the body mass restrial and some arbórea! amphibians. Enscounced in a
per 24 hours at 20°C (Adolph, 1943). Thus, bromeliad with water in the axils of Ihe leaves or wilhin
the amounts of production and loss of met- a moist, rorting log, an amphibian can rehydrate during
abolic water apparently are of minor impor- Ihe day. If sufficienl water is laken in during the day, Ihe
tance in the overall water economy of am- animal can afford to lose water during nocturnal forays.
phibians. For example, the Australian burrowing frog Heleioporus
2. Adult amphibians do not drink, except under eyrei experiences an average waler loss equivalenl lo
certain physiological stresses in a laboratory. 22.3% of ils body mass while it is foraging each night (A.
Thus, the alimentary canal is not an important Lee, 1968).
site of water exchange, except in the degree Although many kinds of amphibians may become ac-
to which water is ingested as a component of tive during and immediately afler heavy rains by day.
(or incidental to) food. Some of this water normally Ihey are active only al nighl; however, the young
may be absorbed in the large intestine, but of some anurans, particularly bufonids, lend lo be diurnal
most is eliminated with the fecal matter. and heliolhermic in conlrasl lo conspecific adulls. On Ihe
3. In air-breathing amphibians, the lungs dissipate olher hand, some groups of anurans characlerislically are
a small and probably fairly constant quantity active only by day. All of Ihese live in habitáis of high
of water into the atmosphere. In habitats of almospheric humidity or Ihose in which water is readily
high atmospheric moisture, this loss would be available. For example, the diurnal Dendrobates and
negligible. In dry environments, the loss could Phylhbates live in forested regions having high almos-
be considerable over a long period of time. pheric humidily, as do mosl species of Colostethus. Olher
4. Aquatic amphibians excrete comparatively large species of Colostethus Ihal live in áreas of lower almos-
quanüties of dilute uriñe; practícally all water pheric humidily are active only in Ihe vicinily of srreams.
loss is via the kidneys. Terrestrial amphibians which Ihey enler frequenlly. Other stream-dwelling frogs
produce urea, and some terrestrial anurans may be rehydrated continuously from the spray of wa-
produce uric acid. lerfalls or by enlering Ihe slreams frequenlly; these in-
5. The vast majority of water lost by terrestrial clude New World bufonids (Atelopus), Asiatic ranids
amphibians is by evaporatíón from the skin. (Staurois), and Australian myobatrachids (Taudactylus).
Rehydration through the skin may occur from Many olher anurans living in cool températe or montane
free water or from the substrate. habilals may be active by day, bul only when Ihere is a
6. Body water can be stored in the urinary blad- sufficienlly posilive moislure gradienl lo overeóme
der and in lymph sacs. Such water provides evaporalive waler loss, unless there is some compellinc
a supply for body tissues as required because reason (e.g., feeding, mating, basking) wherein the anu-
of loss by evaporation, excretíon, or respira- ran risks evaporalive water loss and even death to ac-
tion. complish some goal.
Reduction of Ihe amounl of surface área exposed lo
From these generalities, it is obvious that the significant evaporation is an importanl way of reducing waler loss.
water-conserving mechanisms must involve (1) the cur- Several elongale plelhodontid salamanders and Am-
tailment of water loss through the skin, (2) modificaüons phiuma curl Iheir bodies and lails inlo tighl coils and
of the excretory producís of the kidneys, and (3) storage Ihereby reduce evaporative waler loss (Ray, 1958). Many
of water in vesicles and tissues. Furthermore, survival in arboreal anurans pass Ihe day on branches or leaves of
terrestrial environments necessitates mechanisms for re- brees. By selecting a shaded site and lucking Ihe limbs
hydration. cióse lo Ihe body, and fingers and toes between Ihe body
Because anurans inhábil a wide variety of environ- and Ihe subslrate, tree frogs reduce Ihe surface área ex-
menls and also occur in arid regions, sludies on water posed lo Ihe air and Ihereby reduce evaporative waler
economy have been more extensive on anurans Ihan on loss (Fig. 8-1). Such frogs characleristically are quiescent
salamanders. Liltle is known about caecilians. presumably the slowing of melabolic processes resulte ir.
a slower rale of brealhing and Ihus less loss of moislure
Behavioral Adaptations Ihrough respiration. Eleutherodactylus coqui assume water-
With a few exceplions among Ihe anurans, terreslrial am- conserving poslures on dry nights but are nol quiescen:
phibians generally are noclurnal, Ihereby avoiding higher (Pough el al., 1983).
daytime temperalures and lower atmospheric humidity. Aggregations of recently metamorphosed loads, Bufe
Diurnal retreals of these animáis usually have a higher and Scaphiopus, and subadull salamanders, Ambys-
moisture contení than surrounding áreas exposed lo in- toma, occasionally are found in shellers in dry áreas
 Relationships with the Environment
199

Figure 8-1. Diurnal sleeping posutre

of Agalvchnis caüidryas. Puerto
Viejo, Costa Rica. Photo by W. E.
Duellman.

dosely packed individuáis provide comparatívely less is highly variable (see Chapter 14). Actually, the epider-
sLrface área, overall, for evaporative water loss than do mal sculpturing ¡s important in hydration. Most salaman-
srgie individuáis; Gehlbach et al. (1969) found that iso- ders and all frogs that live in aquatic and riparian situa-
a:ed individuáis of A. tigrinum lost water at a significantly tions have smooth skin on the ventral and lateral surfaces
^cher rate than individuáis in aggregations. Significant of the body. Most terrestrial and arboreal anurans have
rfferences were found between dehydraüon rales of sin- granular skin on the belly and proximal ventral surfaces
¿e individuáis versus aggregates of two to four individ- of the thighs, and many have granular or areolate skin
uáis ofA. macrodactylum (Alvarado, 1967) and between on the flanks. The irregular ventral surfaces provide a
sr.gle versus aggregates of two to five juveniles of three greater surface área that can be in contact with the sub-
=pecies of myobatrachid frogs, Limnodynastes (C. John- strate for greater rates of water absorption, but probably
son. 1969). more important is the habit of flattening the body on a
Many salamanders and anurans utílize burrows made moist surface, thereby spreading the skin and exposing
ry other animáis for diurnal retreats; a few salamanders, the thin skin between the granules to moisture. There
some anurans, and all caecilians créate their own bur- seems to be a general correlation between granular ven-
rows. Such burrowing behavior is best exemplified by tral surfaces and habitáis of frogs. Thus, frogs that char-
anurans in arid habitáis. In Arizona, the spadefoot toad, acleristically are in the vicinity of free water (e.g., Rana,
Scaphiopus multiplicatus, spends about 9 contínuous Ptychadena, Discoglossus, Leptodacfylus) have smooth
rr.onths underground in self-made burrows to depths of venlers, whereas Ihose Ihal are primarily lerreslrial or
90 cm (Ruibal et al., 1969). By maintaining an osmotic arboreal (e.g., Bufo, Hyla, Rhacophorus, Hypero/ius) have
concentration equal to the soil moisture tensión, the toads granular venters. In some large groups inhabiüng diverse
may remain in these burrows for long periods of time environmenls, both types of venters are found in different
•j.ithout losing water to the soil. During the rainy season, species. For example, most species of Eíeutherodactylus
rhese spadefoot toads burrow only about 4 cm for diurnal are terrestrial or arboreal and have granular venters, but
retreats; they emerge each evening. Many anurans bur- members of some groups that characteristically inhábil
row to equal or greater depths during droughts; the deep- margins of streams have smoolh venlers. Mosl hylid frogs
est known burrows are those of the Australian He/eio- have coarsely granular venlers, bul Ihe ventral surfaces
porus eyrei at 80 cm (Bentley et al., 1958). are smooth in Acris, which is semiaquatíc. There are some
exceplions lo Ihe general correlation; Ihe mosl nolable is
Morphological Adaptations Scaphiopus, species of which have smoolh venlers and
Some notable morphological modificatíons, principally of are terrestrial in xeric habitáis. Also, dendrobatids have
the skin, but also of the bladder, are important in water smooth venlers, but Ihese lerreslrial frogs live in humid
economy. foreste or along streams.
The ventral pelvic región has been identified as Ihe
Skin and Cutaneous Vascularization. The skin of área primarily responsible for waler uplake in anurans
amphibians is highly permeable; the presence of mucous (Dole, 1967; R. Baldwin, 1974; McClanahan and R.
glands in the dermis and the vascularizaüon of the dermis Baldwin, 1969). Comparative sludies on Ihe vasculari-
ECOLOGY
200
pectoral cutaneous

dorsal aorta
ventral abdominal

common pelvic-
lateral
cutaneous

ischiatic
lateral ¡schiatic

cloacal ¡schiatíc
Figure 8-2. Vascularization of ventral pelvic regions in anurans. A. Bufo alvarius. B. Xenopus laevis.
Adapted from J. Roth (1973). Banded vessels are arteries; open vessels are veins; solid vessels are those
associated with the integument.

zation of the ventral pelvic región of diverse anurans by .2-

J. Roth (1973) and Christensen (1974) revealed that (1)
the ventral pelvic integument is hypervascularized com- .1-
pared to other regions of the body in terrestrial anurans,
and (2) terrestrial anurans, such as Bufo, have more vas- .3-
cularization in the pelvic región than semiaquatic Rana, .2
which are more vascularized than the aquatic Xenopus .1
(Fig. 8-2). The increased surface área of the integument
and increased vascularity in the ventral pelvic región co- 1.6
incide with behavioral observations and laboratory ex-
periments indicating that this región of the body is most
important in rehydration (Fig. 8-3). Water movement
across amphibian skin is affected by various hormones, Sr
E
of which vasotocin probably is the most significant. The
skin on the ventral pelvic región of anurans is more re-
sponsive to vasotocin than is skin elsewhere on the body
(Bentley and Main, 1972). No comparable regional dif- .51.0
LL

ferentiation of the integument has been identified in sal-

amanders. Moreover, terrestrial and arboreal anurans,
such as Bufo and Litaría, respectívely, have greater re-
sponses to vasotocin than does the aquatic Xenopus.
However, in at least Scaphiopus couchii, responsiveness .6-
to vasotocin is seasonal (Hillyard, 1976b); animáis cap-
tured during most of the year (and tested immediately)
showed no response. .4-
Experiments by Lillywhite and P. Licht (1974) on Bufo
demonstrated that cutaneous channels on the flanks and
dorsum function to move water in all directions over the
surface of the skin; movement seems to occur by capil-
larity. Experiments by López and Brodie (1977) revealed
0' 1 2 3 4 5
that costal grooves function in much the same manner;
Hours
when dry salamanders were placed on a wet substrate,
water moved dorsally in the costal grooves and along the Figure 8-3. Net water flux through isolated pelvic and pectoral
minute cutaneous channels interconnecting the costal skin of anurans. A. Pelvic skin of Xenopus laevis (pectoral skin is
essentially the same). B. Pectoral skin of Bu/o bufo. C. Pelvic skin
grooves. of Bufo bufo. Solid circles are normally hydrated animáis; open
Water absorption should be facilitated by cutaneous circles are dehydrated animáis. Adapted from Christensen (1974 .
 Relationships with the Environment
channels in three ways (Lillywhite and P. Licht, 1974): of the body. Possibly these osteoderms function to de- 201
(1) Any sculpturing increases the surface área of the skin crease evaporative water loss when the frogs are at rest
potentially available for absorbing water. .(2) Channels high in the trees during the day. Atmospheric humidity
induce wetting of an área of skin that is larger than that during the day is much lower in the canopy than it is
in contact with the water source. (3) Forces of capillarity near the ground in rainforests.
attributable to skin structure actually may increase the Evaporative water loss is extremely low in two African
total forcé with which the integument can extract water rhacophorid frogs (Chiromantis petersi and C. xeram-
from a moist surface with which it is in direct contact. pe/ina) that survive long, dry seasons while perched on
Movement of water to the dorsal surfaces of amphib- limbs, trunks, or buildings. These frogs are unique among
ians suggests the importance of cutaneous channels in anurans in having chromatophore units containing múl-
preventing desiccation of integumentary surfaces that are tiple iridophores in the skin of surfaces exposed to desic-
exposed to an ambient atmosphere of relatively low va- cation when the frogs are at rest (Drewes et al., 1977).
por pressure. Any mechanism that supplies water to the A similar chromatophore arrangement is known in the
integumentary surface at rates equal to or exceeding African Hyperolius nasutus, which also has a low rate of
evaporative water losses should be advantageous when evaporative water loss (Withers et al., 1982). In the ab-
pressure gradients from the skin to the ambient atmo- sence of other known morphological structures or phys-
sphere are steep. iological mechanisms to retard evaporative water loss, the
Highly vascularized skin resulte in quantities of blood unique chromatophore arrangement has been suggested
passing near the surface and therefore increased evapo- as the mechanism for reducing water loss, but how this
rative water loss. Several genera of casque-headed hylid might function is not known.
frogs have the skin co-ossified with the dermal bones of
the skull; in these frogs the dermis and its vascularization Urinary Bladder and Lymph Sacs. The urinary
are greatly reduced (Trueb, 1970a). These frogs back bladders in amphibians are baglike structures, but in anu-
into crevices, tree holes, or bromeliads and plug the holes rans they become distended into bilobate structures when
with their heads (Fig. 8-4); thus, only the skin on the they are filled with dilute uriñe. In salamanders, the blad-
head is exposed to the air. Evaporative water loss from ders usually are comparatively smaller than they are in
the skin on the head is much less than that from other anurans; the largest bladder reported in a salamander is
surfaces of the body (Siebert et al., 1974). that of Salamandra salamandra, which contains fluid equal
Some other hylid frogs (e.g., Gastrotheca weinhndü to about 35% of the body weight (Bentley, 1966a). The
and Phyllomedusa bicolor) that inhabit the canopy in bladder of the aquatic Xenopus laevis is small, containing
rainforests have osteoderms in the skin on the dorsum fluid equal to only about 1% of the body weight. How-

Figure 8-4. Blocking of opening between axils

of leaves of a bromeliad by the head of
Gastrotheca fissipes, Santa Teresa, Brazil.
Photo by I. Sazima.
ECOLOGY
202 ever, bladders of anurans that inhábil arid environments Although semiaquatic species normally have access to
can store large quanüties of water. Ruibal (1962b) found free water and all amphibians have access to abundant
that Bufo cognatus can store up to 30% of its body weight moisture during rains, the critical aspects of moisture ex-
as water in the bladder. Australian tree frogs, Litaría to- change with the environment are at times of absence of
topa/mato and L. moorei, can store water equal to 20--30% free water. During these times, amphibians must rely pri-
of their body weight, and this valué in the desert burrow- marily on the moisture contení of the substrate. For ar-
ing frogs, Notaden nicho/si and Neobatrachus wilsmorei, boreal species the source of moisture may be the con-
is about 50% (Main and Bentley, 1964). densation on leaves of bushes and trees, but in terrestrial
The subcutaneous lymph sacs of anurans possibly are species the exchange is with the soil.
another site for water storage. In some burrowing frogs, Soil and moisture availability.—The moisture ten-
the sacs are bloated before the frogs enter the soil for sión of the soil was shown to determine the amount of
long periods of time. The central Australian frog Cyc/o- moisture available to the salamander Plethodon cinereus
rana platycephala is called the water-holding frog: "It by Heatwole and Lim (1961), who introduced three con-
becomes surrounded by loóse, floppy bags of water" cepts: (1) Absorption threshold, which is the level of sub-
(Tyler, 1976:126). However, the lymph sacs are more strate moisture above which mere is a net gain in body
extensive in aquatic anurans than in terrestrial species, weight (uptake of water) by dehydrated amphibians and
so the major function of the lymph sacs may be the col- below which there is a net loss. (2) Critical level, which
lecüon of water from the body üssues (Cárter, 1979). is the level of substrate moisture below which water loss
in amphibians increases markedly. (3) Limiting range.
Physiological Adaptations which includes all valúes of substrate moisture betweer.
The physiological mechanisms associated with water levéis 1 and 2.
economy in amphibians involve reduction of evaporative Absorption of soil moisture involves movement of water
water loss through the skin, increased permeability of the through the soil and transfer of soil-bound water to the
skin at times of favorable moisture tensión, modification skin; this transfer requires cióse adsorption of soil particles
of the excretory products, and osmoregulation. lonic to the skin (Hillyard, 1976a). With a favorable water po-
concentrations and excretory products are controlled tential gradient, water will move across the skin where
largely by the kidneys, which are regulated by neuro- contact allows water movement from soil to skin. With a
hypophysial and adrenal secretions. given absorptive área, water movement across the skin
will be determined by the hydraulic conductivity of the
Moisture Exchange with the Environment. There soil and of the skin. The hydraulic conductivity of sub-
have been many studies on the rates of water loss and saturated soil increases as the water contení (and water
water uptake in amphibians, especially anurans. How- potential) increases. In wetter soils, the hydraulic con-
ever, the results of mese studies are not necessarily read- ductivity of the soil is greater than that of the skin, and
ily comparable because of differences in experimental water movement will be greatest across the skin havinc
design. For example, water loss (usually determined as the greatest conductivity. In drier soils, the hydraulic con-
weight loss) has been measured in süll air or at relatively ductivity of the soil is lower than that of the skin, and
rapid rates of convection; also, bladder contents were water movement in either direction across the skin is greai.
emptied in some experimental animáis and not in others. diminished. However, over a long period of time, ever.
In experiments dealing with rehydration, the absorptive a slow rate of water loss would be lethal. Amphibians
capabilities of the skin on different regions of the body that pass many months burrowed into relatively dry SOL
and the moisture tensión of the substrate were not always can elévate the osmolarity of their body fluids and theretx
taken into consideration. Nevertheless, some patterns are decrease water loss, or some form a waterproof cocooa
evident, and some generalities can be made. Some experiments have related soil particle size and
Unless the skin of amphibians is protected by some the affinity of the soil particles for water (soil matric po-
special coating essentially "waterproofing" the skin or tential) with water absorption rates. The effect of soil ma-
contains structures that reduce the permeability, the skins tric potential on the water economy of spadefoot toads.
of amphibians, irrespective of taxonomic group or habi- Scaphiopus couchii and S. multiplicatus, was examined
tat, give up water at approximately the same rate when by Ruibal et al. (1969), Shoemaker et al. (1969), and
exposed to equivalen! conditions of desiccation. On the McClanahan (1972). Soils of fine particle size have a
other hand, rehydration rates are highly variable and de- higher affinity for water than do sandy soils with idéntica;
pend on structural differences and absorptive properties water contení. Therefore, it is more difficult for anurans
of the skin; these seem to be related to habitat—terrestrial to obtain water from silty soil than sandy soil when the
and arboreal species have faster rates of rehydration than water contení is low.
semiaquatic and aquatic species (see Mullen and Alvar- Absorption thresholds have been determined for few
ado, 1976, and P. Brown etal., 1977, forreviews). How- species. Heatwole and Lim (1961) found the absorptior
ever, aquatic species can tolérate prolonged hydration threshold for Plethodon cinereus to be very low, 1.0 to
better than terrestrial species. 1.5 atmospheres of soil moisture tensión. Six species c:
 Relationships with the Environment
si2_~anders studied by Spight (1967a) had absorptíon 203
teesholds of about 2 atm (Fig. 8-5), but Spotila (1972)
• 2 study of 14 species of plethodonüd salamanders
istr.d that thresholds varied from 1.2 to 2.8 atm. R.
Kaker and Whitford (1970) reported thresholds of three
•csorial anurans (including Scaphiopus mitltiplicatus) to
se about 2.5 atm, Bu/o americanus 1.5 atm, Hyla cinérea
12 atm, and Rana pipiens 0.8 atm. However, Ruibal et
a. 1969) reported the absorption threshold of S. mu/-
ípácotus, which spends about 9 consecutíve months bur-
•jaKd in soil, to be above 10 atm, and it may be as high
atm; the absorption threshold varíes depending on
±e soil moisture tensión and the animal's interna! os-
Tcic concentration. Thus, it seems that absorption
±resholds are highest for amphibians that are subjected
c A-ater stress in nature.
Dole's (1967) work on Rana pipiens showed that these
srrJaquatic frogs could absorb water from wet soils and
rtm sand having a water content of 20%, but frogs that
tere rehydrated on sand containing only 10% water could
-o: regain all of the water that they lost by dehydration. -240
~-.e arid-adapted Australian anuran Heleioporus eyrei
2 4 6 8 10
sríorbs water from sand containing 13% water (Packer,
Soil Water Content (%dry weight)
1963), and Scaphiopus mu/tip/icatus can do the same in
scils containing only 3% water (Ruibal et al., 1969). Figure 8-5. Relationship between soil water content and rate of
Temperature and moisture exchange.—Most exper- water exchange by six species of salamanders (solid circles). The
soil moisture tensión at various water contents is shown by open
ir.ents dealing with dehydration and rehydratíon were circles (each is the mean of three valúes). Based on data in Spight
rKrformed at constant temperatures. Claussen (1969) (1967).
found no correlations between rehydration rates and
smperature in six species of North American anurans.
AJthough hormonal reléase and rate of blood circulation Size, surface área, and moisture exchange.—Intra-
r.crease with temperature, other properties of anurans, specific differences in tolerance to water loss do not seem
sspecially differential uptake of water by the skin in dif- to be related to size in some species. For example, no
fcrent regions of the body, seem to negate the effect of significant correlations between size (measured as standard
temperature. Experimental design has affected the results weight) and tolerance to water loss were found in indi-
DÍ many experiments. Animáis usually are rehydrated from viduáis among several species of North American hylids
a moist substrate; at higher temperatures evaporative water and ranids (W. Schmid, 1965; Farrell and MacMahon,
joss may balance or exceed the rehydration rate. 1969; Ralin and Rogers, 1972). However, differences in
Spotila (1972) demonstrated significant differences in rates of evaporative water loss probably relate most closely
both dehydration and rehydration rates at different tem- to surface-area/volume ratios. With the exceptíon of a
peratures in species of plethodonüd salamanders. De- few species of frogs having integumentary modifications
hydration was accompltshed in desiccators and rehydra- that reduce the rate of evaporative water loss, this rate
tion in culture dishes partially filled with water, both per unit área of skin seems to be about the same in all
maintained in environmental chambers at 5,15, and 25°C. species subjected to equivalent experimental condiüons.
Both rates were positively correlated with temperature, Passage of dry air over an amphibian results in evapo-
and the rehydration rate showed a greater response to ration from all exposed surfaces; small amphibians have
temperature, except for one species that had the same proportionately more surface área and, therefore, have
rates (Fig. 8-6). higher rates of evaporative water loss. This was dem-
Dermal mucous glands discharge secreüons more fre- onstrated among species of plethodontid salamanders by
quently at higher temperatures, and the layer of mucus Spotila (1972). For example, the dehydration rate of
on the skin increases the rate of evaporative water loss, Plethodon cinereus (mean weight 0.62 g) was 10 mg •
whereas dry skin forms a diffusion barrier and a decrease cm~ 2 • h" 1 , whereas in P. glutinosas (mean weight 3.93
in the rate of evaporative water loss (Lillywhite, 1971a). g) subjected to the same experimental conditíons the rate
Dehydrating amphibians at high temperatures seem to was 3 mg-cm" 2 ^" 1 . Heatwole et al. (1969) subjected
be faced with conflicting physiological demands—how to E/eutherodacty/us portoricensis to various experiments and
decrease the rate of evaporative water loss and also lower found a significant negative correlation between body
body temperatures (see section: Thermoregulation). size and rate of evaporative water loss. Also, a significant
ECOLOGY
204
= 12-
Dehydration Rehydration

c
CD 8
O

S 6-

o .
•53 4
Figure 8-6. Dehydration and rehydration rates
of plethododontid salamanders acclimated to o
three temperatures. Open circles = Eurycea OJ 2-
lucífuga; open squares = Plethodon caddoensis; 03
salid Mangles = P. glutinosas; solía cacles = CC
P. jordani; solid squares = P. ouachitae; open
triangles = P. yonahlossee. In the dehydration
graph P. yonahlossee is the same as P. 15 25 5 15 25
glutinosas. Adapted from Spotila (1972). Acclimation Temperature (°C)

negative correlation was found to exist between the rate mal. Nocturnal species had the peak of activity at nighL
of evaporaüve water loss and body mass among species whereas diurnal species had a peak of activity by day. A
of "waterproof frogs (Withers et al., 1982). notable exception was Litaría caerulea, in which diurna!
Activity and moisture exchange.—A dehydrating and nocturnal peaks were nearly identical.
amphibian faces conflicting drives. In order to escape
desiccating conditions, it must increase its acüvity at the Waterproofing. Some amphibians have developec
cost of increasing its evaporaüve water loss. If the animal novel ways of "waterproofing" the skin, either by the
assumes a water-conserving posture, it can reduce formation of a cocoon that encases the body during long
evaporative water loss and prolong its ability to survive, periods of dormancy or by the secretion of a coating
but it will not be able to escape if the desiccating con- having iow permeability that covers the animal during
ditions persist. In at least one anuran, Notaden bennetti the day, when it is inactive.
(Heatwole et al., 1971), and one salamander, Plethodon One salamander, Siren intermedia, and several species
cinéreas (Heatwole, 1960), activity (mostly escape be- of anurans living in xeric habitats are known to form
havior or movements along moisture gradients) increases cocoons encasing the body while the animal is in a sub-
during progressive dehydration until a peak is reached, terranean burrow. Siren intermedia burrow into the mud
after which activity declines (burrowing or moisture-con- at the bottom of drying ponds; once ensconced in their
serving postures) until just before death, when a brief, burrows, sirens form a parchmentlike cocoon that com-
secondary burst of activity (escape movements) occurs. pletely envelops the animal, except for the mouth (Rene
Heatwole et al. (1969) showed that activity greatly influ- et al., 1972).
ences the rate of evaporative water loss in Eleutherodac- Burrowing anurans that form cocoons include Pter-
tylus portoricensis. In that species, activity increases nohyla fodiens in North America (Ruibal and S. Hillman.
evaporative water loss up to 200% above the rate for 1981), Ceratophrys omata and Lepidobatrachus llanen-
individuáis at rest, largely by changes in exposed surface sis (Fig. 8-7) in South America (McClanahan et al., 1976).
área (máximum effect 130%) and gradient modifications Pyxicepha/us adspersus and Leptopelis bocagei in South
(máximum effect 30%); effects of elevated metabolism África (Loveridge and Craye, 1979), and Limnodynastes
probably account for the rest. spenceri, Neobatrachus pictus, and several species of Cy-
R. Putnam and S. Hulmán (1977) showed a progres- clorana in Australia (A. Lee and Mercer, 1967).
sive increase in activity levéis in Bufo bóreas and Xen- The cocoon, composed of layers of statum corneum.
opus taevis during dehydration, up to 35% and 25% loss is dry, parchmentlike, and encases the entire frog, with
in body weight, respectively. Experiments by Heatwole openings at the nostrils. In Ptemohyla fodiens the cocoon
and Newby (1972) on 12 species of anurans showed that is about 0.05 mm thick and is formed by múltiple shed-
peak activity levéis occurred at the loss of 31 to 40% of dings of the epidermis (Fig. 8-8); as many as 43 layers
body weight to dehydration in 11 species, but that the of epidermal cells, each layer separated by an intracel-
peak for juvenile Bufo marinus was 41 to 50%. Further- lular space representing the original subcorneal space.
more, Bufo marinus maintained activity when its body were observed (Ruibal and S. Hillman, 1981). The co-
water contení had been decreased to 30 to 39% of nor- coon of Lepidobatrachus //anensis may contain as many
 Relationships with the Environment
205

Figure 8-7. South American

burrowing frog Lepidobatrachus
llanensis in a cocoon (left) and
emerging from a cocoon upon
rehydration (right). Photos by L. L.
McClanahan.

nohyla and Lepidobatrachus are immobile during cocoon

formaüon. This immobility allows the detached stratum
corneum to remain in place and the next, and subse-
quent, sheddings also to remain and to adhere to each
other by means of the secreted subcorneal mucus, thus
providing the multilayered, protective cocoon.
Experimental passage of dry air over cocooned indi-
viduáis of Pyxicepha/us adspersus and Leptope/is boca-
gei showed that weight loss (water loss) was reduced to
50% and 20%, respectívely, of the loss by noncocooned
frogs (Loveridge and Craye, 1979). Comparable figures
for Lepidobatrachus llanensis are 7—14% (McClanahan
et al., 1976). Equivalen! rates of water loss were calcu-
lated for cocooned individuáis of Pternohyla fodiens and
Australian myobatrachids (A. Lee and Mercer, 1967;
Ruibal and S. Hulmán, 1981). Rates of evaporative water
loss in nature certainly are lower than those obtained in
the laboratory. The experimental conditions of passing
dry air over cocooned frogs are far more severe than
those encountered in subterranean burrows (Fig. 8-9).
Experiments with the salamander Siren intermedia by
Gehlbach et al. (1973) revealed that individuáis in co-
coons lost 25-28% of their body weight during a 16-
week period; sirens die if they lose 40-60% of their body
weight.
As more epidermal layers are added, the cocoon be-
comes thicker and less permeable. Laboratory experi-
Figure 8-8. Electron micrograph of a section through the cocoon ments with the frog Lepidobatrachus llanensis by Mc-
of Pternohyla fodlens. Scale = 1 |im. Photo courtesy of R. Ruibal. Clanahan et al. (1983) showed that individuáis add an
epidermal layer daily for 40 days, and that there is an
inverse relationship between the number of layers and
as 60 layers (McClanahan et al., 1976), and that of Pyxi- the rate of water loss. During 35 days the evaporative
cepha/us adspersus, 36 layers (Loveridge and Craye, water loss dropped from 8.0 mg-g"1^"1 to 0.9
1979). Reno et al. (1972) suggested that the cocoon of mg-g-^rr 1 .
Siren was formed by the hardening of mucus secreted In some tree frogs of the genus Priyí/omeduso, dermal
by the dermal mucous glands. However, the microscopic secretions provide a covering that reduces evaporative
structure of the cocoon is the same as that of cocoons of water loss to 5-10% of that of most other anurans and
anurans. comparable to that of a desert-adapted lizard (Shoe-
Normal shedding in anurans is arrested by hypophy- maker et al., 1972; Shoemaker and McClanahan, 1975).
sectomy (Budtz, 1977); hypophysectomized toads de- These frogs (P. boliviana, hypocondrialis, iheríngi, and
velop a multiple-layered stratum corneum. At least Pter- sauuagei) inhábil subhumid Bolivia, and arid áreas in
ECOLOGY
208 (Loveridge and Withers, 1981). Although data are avail-
able for few species, it is evident that the water economy
of amphibians subjected to dehydration benefits from in-
5-
creased concentrations of certain electrolytes, especiallv
sodium and chloride.
I These electrolytes also are stored in body tissues.
4- Shoemaker (1964) found that the concentration of po-
tassium was much higher in the skeletal muscle and liver
o than in the plasma of Bu/o marinus and that the con-
3- centrations of sodium and potassium increased at aboui
c the same rates in tissues and plasma in dehydrated in-
CD
O dividuáis, but there was an initial decrease in the con-
o 2- centration of potassium in the blood. Experiments or.
o
CD physiological adaptations of Rana cancriuora to salinity
CO
by M. Cordón and Tucker (1968) revealed that much
_CD
greater amounts of potassium were stored in skeletal
0_
1-
muscle than in plasma, and concentrations of all electro-
lytes in plasma and muscle tissue increased at about the
same rates at higher salinities of the external médium
However, changes of concentrations of intracellular urea
TapH20 10 15 20 25 and free amino acids are primarily responsible for in-
External Médium (10mM/l NaCI) creases in osmotic concentrations in skeletal muscle
Figure 8-11. Mean contributions of measured osmolytes to Subsequent experiments on Ambystoma tigrinum (Del-
plasma osmotic concentration in Xenopus laevis adapted to various son and Whitford, 1973b) showed that there were two
concentrations of salt water. Redrawn from Romspert (1976).
major alterations of body fluid concentrations during long-
term dehydration—an initial increase in concentrations
of electrolytes and a subsequent increase in urea.
characteristic of arboreal anurans—9.5 to 21 times the Numerous studies have demonstrated the ability oí
concentration in various hylids and the rhacophorid Chi- amphibian skin ¡n situ or in vitro to take up sodium anc
romantis petersi (Shoemaker and McClanahan, 1975; chloride from an aquatic médium (see Salibián, 1977.
Drewes et al., 1977). The greatest increase reported is in for review). Apparently urea must be present in the plasma
A. tigrinum; individuáis increased the urea concentration for ion transfer to take place and build up the concen-
from 10 mOsm/liter of urea in hydrated controls to 100 tration of electrolytes; the changes in the electrical prop-
to 330 (mean = 220) mOsm/liter in individuáis dehy- erties of isolated amphibian skin in the presence of urea
drated in soil for 9 months (Delson and Whitford, 1973). presumably actívate an inward catión pump or an OL:
Spadefoot toads, S. couchii, also store urea in muscle ward anión pump (M. Cordón and Tucker, 1968).
tissues (McClanahan, 1964), and muscle tissue of the The source of urea and electrolytes in feeding am-
euryhaline R. cancriuora is able to tolérate high concen- phibians is from the metabolism of the proteins in their
trations of urea (Thesleff and Schmidt-Nielsen, 1962). food, but individuáis that are resisting desiccation by re-
Concentration of electrolytes vanes considerably among maining in burrows or cocoons for long periods of time
hydrated amphibians, with levéis of sodium (Na + ) and or are faced with increasing salinity but no food mus
chloride (Cl~) always at least 10 times greater than the catabolize body proteins (Shoemaker and McClanahan.
level of potassium (K + ). In animáis subjected to water 1975; Romspert, 1976). Water stored in the urinary blac-
stress, the concentrations of sodium and chloride show der also can aid in osmoregulation, for the bladder wals
marked increases, but that of potassium may increase or are permeable to urea and also transport sodium (Ben:-
decrease (Fig. 8-11). For example, among aquatic and ley, 1966b).
semiaquatic anurans (Xenopus laevis, Bufo virtáis, Rana
cancriuora) exposed to concentrations of 40 to 50% sea Renal Function. Amphibian kidney function has beer.
water for 3 to 7 days, sodium showed an increase of 39 investigated thoroughly (Deyrup, 1964). Because ot
to 61%, chloride 51 to 119%, and potassium 3 to 50% pressure differentials, fluid is filtered from the blood plasme
(M. Cordón et al., 1961; M. Cordón, 1962; M. Ireland, through capillary walls in the glomerulus and into the
1973). The increases in various hylids and Chiromantis kidney tubule. By a combination of pressure and ciliar.
petersi generally are comparable to the foregoing figures: action, the fluid is forced down the tubule. Cells lininc
sodium 22 to 90%, chloride 17 to 94%, and potassium the lumen resorb water and solutes; these pass back in::
41 to 93% (Shoemaker and McClanahan, 1975; Drewes the blood flowing through capillaries surrounding the tu-
et al., 1977). In hydrated versus cocooned Pyxicephalus bule. Simultaneously, urea and other solutes are secrete;
adspersus, sodium increased 42% and potassium 59% from the blood into the tubular fluid. Water resorptior
 Relationships with the Environment
:cr_rs primarily in íhe proximal convoluled lubule. Coe- rhacophorid frogs of the genus Chiromantis are uricotelic 209
;•—.: fluid can enler íhe renal lubules via ciliated neph- (Shoemaker and McClanahan, 1975; Drewesetal., 1977).
--rimes in salamanders and thus may add lo the glo- In these anurans the partitioning of water into various
--;-_ar fíltrale. In anurans the nephrostomes connecl lo producís is independen! of water turnover, and most of
r-: renal veins, and Ihey may play a role in waíer re- the nitrogen is excreted in the form of precipitated urate
.-:—ion from íhe bladder. Perilubular circulation is de- salts. When uricotelic frogs are maintained out of water
3i.ec from the efferení glomerular arterioles and from and fed, precipitated urate accumulates in the bladder,
3EraI portal veins. The kidneys are nol capable of pro- thereby indicatíng continued renal functíon during water
•ong hypertonic uriñe. deprivation. At least in Phy//omedusa sauuagei, urate ex-
This lype of slruclure is admirably suited for life in fresh cretion prevenís the rapid concentratíon of urea in íhe
T. for all amphibians can produce dilute uriñe al very body fluids and also aids in eleclrolyle excrelion; 45% of
i rales (10-25 ml-kg" 1 ^" 1 ) when mainlained in fresh íhe sodium inpuí and 22% of íhe polassium inpul are
• (Shoemaker and Nagy, 1977). In this situatíon glo- secreíed in urale form. Uricoíelism combined wilh low
• filtration rales are high (20-50 ml-kg-^h" 1 ) and rates of evaporative waíer loss places these arboreal anu-
can be considerably higher in experimenlally waler-loaded rans in a positíon similar to that of insectívorous lizards
animáis. In anurans, only aboul half of íhe waíer is re- in íerms of their ability ío osmoregulaíe wiíhoul access
aarbcd in the lubules, bul resorptíon of sodium and chlo- ío fresh waíer.
adc may be aboul 99% complete (Garland and I. Hen- J. Balinsky eí al. (1976) determined differences in en-
easen, 1975). In larval salamanders, glomerular filtration zymes of urea and uric acid metabolism between the
q»p* tend lo be lower (8-16 ml-kg" 1 ^" 1 ), bul only 10 uricotelic anuran Chiromantis xerampe/ina and ureotelic
r> 30% of the filtered water and 90 to 95% of the filtered amphibians. They concluded thaf íhe adapíation ío uri-
sodium are resorbed when íhe animáis are in fresh water colelism involves íhree kinds of enzymalic changes: (1)
¡Krschneretal., 1971; Stiffler and Alvarado, 1971). When Levéis of íhe enzymes of íhe urea cycle are lowered; íhis
fie concenrration of the environmental médium is in- evidently is correlated with the decreased ouípuí of urea
oeased or the animáis are deprived of water, glomerular and presumably represenís an economy measure, re-
flrration rates are reduced drastically, fractional water re- ducing íhe synthesis of enzymes not needed for metabo-
sorption increases markedly, and íhe concentration of íhe lism. (2) Levéis of íhe enzymes for uric acid degradalion
uriñe approaches Ihat of the plasma. Renal water con- are lowered; íhis is vilal because il ensures Ihal íhe uric
servation is well developed in amphibians because Ihey acid formed in íhe kidneys and liver is nol degraded inlo
can become completely anuric after loss of only a small urea. (3) There is an increase in the level of al leasl one
Sraction of their body water. Generally il is assumed Ihal enzyme for uric acid biosynlhesis (PRPP amidolransfer-
^omerular fillration ceases, but analysis of kidney func- ase). This model of urea and uric acid melabolism re-
áon is difficult when no uriñe is produced. quires íhe acquisitíon of no new enzymes but only a
Energetícally, ammonia is the most economical vehicle change in existing enzymatic palhways.
for nitrogen excretion, bul ils loxiciry precludes íhis prod-
ucl when water turnover is low. On the basis of equivocal Hormonal Effects. The neurohypophysis produces
evidence, Jungreis (1976) suggested thal íhe main ad- lwo identified hormones (arginine vasotocin and oxylo-
vanlages of excretion of ammonia by aquatic amphibians cin) Ihal affecl osmoregulalion direclly. These hormones
are in catión conservation and pH regulation. Most am- (and also mammalian neurohypophysial peptídes) in-
phibians are ureotelic, but they excrete appreciable crease the permeabilily of íhe skin and membranes of
amounls of ammonia when Ihey are in water and be- íhe urinary bladder and kidney tubules, Ihereby accel-
come completely ureotelic when water influx is low. Re- eratíng the diffusional uplake of free waíer and hypotonic
duction or cessation of uriñe production leads lo an ac- uriñe in the urinary bladder and kidney tubules (Deyrup,
cumulation of urea, which places íhe animal in a more 1964). However, some aquatic salamanders (Necturus,
favorable siluation for oblaining water from soil or saline Amp/iiuma, Siren, and Desmognathus quadramacu/aíus)
solutions. Accumulated urea is eliminaled rapidly by íhe have limiled responses lo arginine vasolocin; nol all aquatic
kidneys when íhe animáis are rehydrated. There is active, salamanders respond in íhe same way, for íhe aquatic
tubular secretion of urea, but when plasma levéis of urea newts (Notophíha/mus and Triíurus) have a slrong re-
are high, urinary urea concentrations usually approxi- sponse (P. Brown el al., 1972). Xenopus /aeuis is unique
male Ihose in íhe plasma. This is rrue even for Rano among anurans studied in that arginine vasotocin in-
cancriuora adapled lo saline conditions, where active tu- creases water uptake by the skin bul apparenlly does nol
bular resorptíon of urea would be beneficial (Schmidt- suppress uriñe formation (Ewer, 1952).
Nielsen and P. Lee, 1962). In this situation uriñe flow Adrenaline stímulates active transport of chloride from
rales are reduced greally (malching osmolic influx) by the inside to íhe oulside of isolaled frog skin and also
reducing íhe glomerular fillration rale by aboul 75% and affecls glomerular circulalion and filtration. Inlerrenal se-
resorbing more Ihan 90% of the fíltrate. cretions of aldosterone and cortisol effect renal sodium
Several hylid frogs of the genus Phyí/omedusa and two excretion and sodium transport by the urinary bladder
ECOLOGY
210 (Chester Jones et al., 1972). Deoxycorticosterone glu- tion to or from the substrate, (3) thermal radiatíon to the
coside enhances sodium transport by the skin of Bufo environment, and (4) evaporatíve heat loss. A basking
(Pasqualini and Riseau, 1951). anuran also receives heat from direct sunlight and from
The reléase of all of these hormones initially involves thermal radiatíon from the atmosphere, substrate, and
the preoptic nucleus of the hypothalamus, which stim- vegetation nearby.
ulates the neurohypophysis. This stimulation results ¡n
the reléase of the neurohypophysial hormones that di- Thermal Tolerance
rectly effect osmoregulation and the secretions that actí- Amphibians as a group have a wide range of thermal
vate the adenohypophysis, causing it to reléase adreno- tolerances; differences in tolerances reflect the different
corticotropic hormone (ACTH). This hormone stimulates thermal regimes in their habitáis. However, individuáis
the interrenal bodies to reléase aldosterone and cortísol. can be acclimated to different thermal regimes that result
In at least some anurans, dehydration causes the reléase in modifications of their tolerances.
of the neurohypophysial secretíons (Bentley, 1974), but
the specific neurophysiological mechanisms that initiate Thermal Requirements. The temperatures at which
hypothalamic activity are not known. amphibians are active in the field are known for many
species of salamanders and anurans, especially species
in North and Central America (Brattstrom, 1963; Peder
TEMPERATURE et al., 1982). As a group, anurans usually are active at
Amphibians are ectotherms, and generally have body temperatures exceeding the activity temperatures of sal-
temperatures cióse to that of their immediate surround- amanders (Table 8-1). On the basis of the data on North
ings, especially the substrate. There is no evidence of and Central American amphibians, the range of temper-
intemal heat-productíon mechanisms that increase the atures for salamanders is -2.0 to 30.0°C
body temperatures of amphibians above that of the en- (mean = 13.9°C), compared with 3.0 to 35.7°C
vironment. The amount of metabolic heat produced is (mean = 21.7°C) in anurans. This difference becomes
so small that it is lost immediately to the environment even more evident if the data for the cold-adapted As-
(Fromm, 1956). Some anurans bask and thereby raise caphus are not included; the mean temperatures for anu-
their body temperatures; however, basking creates prob- rans, exclusive of Ascaphus, is 23.6°C.
lems of evaporatíve water loss. In warm environments, Complex relatíonships exist between body tempera-
most amphibian behavior seems to be associated with tures and latitude and altitude. For example, Peder and
maintaining low body temperatures, but cryptic and noc- J. F. Lynch (1982) found that ambystomatíd and pleth-
turnal activity (in places or at times of lower tempera- odontid salamanders in the températe zone experience
tures) more likely is a response to problems of water lower minimum temperatures than neotropical salaman-
economy than to temperature. ders. The tropical salamanders show similar rates of de-
In cryptic or nocturnal amphibians the thermal rela- cline in mean body temperatures with increasing altitude.
tionships with the environment involve (1) convective but the temperatures of ambystomatids at high altitudes
heat loss or gain from the atmosphere, (2) heat conduc- are significantly higher than those of plethodontids at the

Table 8-1. Temperatures of North and Central American Amphibians Recorded in the Field*
Number Temperatures ("O
Group Species Individuáis Range Mean
Salamanders
Cryptobranchids, amphiumids, sirenids 5 12 8.0-28.0 20.1
Salamandrids 4 109 4.5-28.4 16.0
Températe ambystomatids 9 933 1.0-26.7 14.5
Tropical ambystomatids 12 56 10.5-30.0 19.0
Températe aquatic plethodontids 9 261 2.0-22.0 11.3
Températe terrestrial plethodontids 28 2065 -2.0-26.3 13.5
Tropical plethodontids 43 1660 1.8-30.0 14.2
Anurans
Ascaphus 1 5 4.4-14.0 10.0
Scaphiopus 2 11 12.2-25.0 21.4
Leptodactylids 5 11 22.0-28.0 24.7
Bu/o 17 474 3.0-33.7 24.0
Hylids 14 507 3.8-33.7 23.7
Gastrophryne 2 108 15.5-35.7 26.5
Rana 12 299 4.0-34.7 21.3
*Based on Brattstrom (1963) and Peder et al. (1982).
 Relationships with the Environment
same altitudes. Because they are aquatic, the ambysto- the presence of relatively large quantities of glycerol in 211
matids presumably are not subjected to temperatures as body tissues and fluids in these frogs in the winter; glyc-
variable as those encountered by the terrestrial pletho- erol was not present in the frogs in the summer, ñor at
dontids. Brattstrom (1968,1970) found that tropical anu- any time of the year in Rana septentrionalis and R. p¡-
rans have a higher thermal regime trian do anurans in piens, two species that cannot survive freezing temper-
the températe zone and that species (or populations) at atures.
high altitudes have lower thermal regimes than do those In nature, many amphibians seem to be active at char-
at low altitudes. Intraspecific differences in thermal tol- acteristic levéis of body temperature, and it is commonly
erances may occur over short geographical distances with assumed that these levéis invariably represent the actual
a drastic change of alütude, as noted for populations of thermal preferences of particular species. However, the
the chorus frog, Pseudacris tríseríata, on the eastern face range of body temperatures over which at least some
of the Rocky Mountains in Colorado, by K. Miller and species are active in nature markedly exceeds or differs
Packard (1977). from those observed in thermal gradients in the labora-
Seasonal variation in body temperatures is greater tory. Consequently, field measurements may not define
among températe amphibians than among tropical spe- levéis of body temperature actually preferred for activity.
cies. However, at a given time and place, variation in For example, Peder (1982b) found that the mean tem-
body temperatures among members of a population is peratures selected on a thermal gradient by six species
similar for températe and tropical amphibians. Species of plethodontid salamanders were 1.1 to 5.7°C
living at high altitudes are subjected to highly variable (mean = 3.7°C) lower than the mean temperatures of
temperatures daily, whereas those in warm tropical re- individuáis from the same localities in nature, as given by
gions have relatively little daily variation in temperature. Peder et al. (1982). Not all data are in agreement; for
Species living at high altitudes in the low latitudes ex- example, Lillywhite (1971a) found that preferred body
perience diel temperature variations approximating the temperatures of juvenile Rana catesbeiana on a thermal
annual variation. gradient in the laboratory were essentially the same as
The majority of field data suggest that amphibians sel- those in nature.
dom maintain a constant body temperature in the man- Although amphibians seem to avoid extremes and ex-
ner of some reptiles (Huey and Slatkin, 1976), but rather hibit thermal preferenda, the preferred body tempera-
are at whatever temperatures are available within suitable tures may be altered by trophic state, acclimation tem-
microhabitats. The covariance of body temperatures with perature, developmental stage, environmental moisture,
the environment is evident at the level of individuáis, oxygen availability, reproductive state, time of day, and
populations, and species (Carey, 1978). Therefore, most availability of appropriate environmental temperatures
amphibians seem to maintain a constant body temper- (Peder (1982b). Of all these factors, moisture probably
ature from day to day only when the prevailing environ- has the most notable effect. In Spotila's (1972) study,
mental conditions do not vary. For example, the similar salamanders selected the highest relative humidity in
body temperatures of amphibians living in bromeliads in thermal and relative humidity gradients. Thus, there seems
the tropics (Peder, 1982a; Peder and J. F. Lynch, 1982) to be a definite interplay between thermal and moisture
are the result of minimal thermal diversity within the bro- responses.
meliads. Likewise, the body temperatures of the lepto- Preferred body temperatures usually are nearer the
dactylid frog Somuncuria somuncurensis are limited to upper than the lower extremes of temperature tolerated.
the nearly constant temperatures (20-22°C) of the ther- Brattstrom (1968) recorded the critical thermal máxima
mal springs in which it lives (Cei, 1969). for six species of North and Central American anurans
A few salamanders have been found active at tem- to be greater than 40°C, notably higher than the tem-
peratures near 0°C; these include Hyaromantes platy- peratures at which these species are active in nature
cephalus at - 2°C (Brattstrom, 1963), Eurycea multipli- (Brattstrom, 1963); preferred temperatures were far above
cata at 0°C (P. Ireland, 1976), Ensatina eschscholtzi at the minimum temperatures tolerated, For example, tem-
1°C (Stebbins, 1954), and Ambystoma jeffersonianum peratures of 19 active Smilisca baudinii were 21.2 to
and A. maculatum at <1°C (Peder et al., 1982). The 28.8°C (mean = 24.3°C), whereas the critical thermal
lowest temperatures for anurans are 3.0°C for Bufo bó- máximum and minimum were 40.4 and 5.0°C, respec-
reas (Brattstrom, 1963) and 3.5°C forB. bocourti (Stuart, tively. Comparable temperatures for 25 Bu/o marinus
1951). Mullally (1952) determined that -2°C was the were 22.0 to 27.0°C (mean = 25.2°C) with critical ther-
lethal minimum temperature for B. bóreas. mal máximum and minimum of 41.8 and 11.0°C, re-
Many physiologists discounted the possibility of am- spectively. The highest critical thermal máximum for sal-
phibians surviving if frozen. However, W. Schmid (1982) amanders (38°C for Ambystoma mabeei; V. Hutchinson,
reported that three species of anurans (Hy/a crucifer, H. 1961) is 8°C above the highest temperatures recorded in
versicolor, and Rana selvática) could tolérate tempera- the field (see Table 8-1); a similar difference is found in
tures of - 6°C for 5 days, at which time approximately anurans, the highest critical thermal máximum for which
35% of their body fluids was frozen. He demonstrated is 42.5°C for Hy/a smiíhii (Brattstrom, 1968).
ECOLOGY
212 Table 8-2. Comparison of Criücal Thermal Máximum Temperatures Determinad by the Onset of Spasms of Anurans from Températe North
America and Tropical Middle America Acclimated to Different Temperatures for 2 or 3 Weeks0

Number Acclimation Critica! thermal Range of

Group of species temperature (°C) máximum (°C)b variation (°C)

Températe anurans 27 5 28.1-3.74 (32.6 ± 2.47) 9.3

15 23 31.3-40.0 (35.3 ± 2.57) 8.7
18 30 33.6-40.3 (36.3 ± 1.92) 6.7
Tropical anurans 4C 5 31.5-36.7 (34.3 ± 2.20) 5.2
6 23 31.4-40.0 (37.2 ± 3.15) 8.6
6 30 39.5-42.5 (40.7 ± 1.20) 3.0
"Based on data in Brattstrom (1968).
'Numbers in parentheses are means ± 1 standard deviation.
'Individuáis of 15 additional species died at this acclimatory temperature.

Thermal Acclimation. Amphibians usually respond

to a prolonged change in ambient temperature by ad-
justing their thermal tolerances accordingly. This com- CJ

pensatory change is known as thermal acclimation. Nu-

merous investigators of thermal acclimation in amphibians I 39-
£
have used the critical thermal máximum (CTMax) or (far
less commonly) minimum (CTMin) as the measure of 38- SOdays
temperature tolerance at which 50% of the animáis sur- "ro
vive. For data on salamanders, see V. Hutchinson (1961),
Claussen (1977), Layne and Claussen (1982), and ref-
erences cited therein; for data on anurans, see Brattstrom ro
(1968, 1970, 1979) and references cited therein. Most o
~ 36-1
investigators have been concerned primarily with the ú
magnitude of thermal acclimation, but acclimation rates
have been considered by some workers, notably Bratt-
strom and Lawrence (1962), Brattstrom and Regal (1965),
V. Hutchinson and Rowlan (1975), Claussen (1977), and Days
Nietfeldt et al. (1980). Figure 8-12. Comparison of rates of thermal acclimation of newts,
The experimental approach usually consists of accli- Notophthalmus viridescens. Symbols are means of samples. Gíreles
matíng individuáis to a constant temperature and then are for individuáis transferred from 4 to 20°C; squares from 19.5 to
32°C; Mangles from 20 to 4°C. Redrawn from V. Hutchinson
increasing or decreasing the temperature to determine (1961).
the critical thermal máximum or minimum that the ani-
máis can tolérate. Criücal temperatures usually are de-
termined by the onset of spasms, loss of righting re- salamanders (e.g., Notophthalmus uiridescens; Fig. 8-12)
sponse, and heat or cold vigor. Equivocal results obtained and anurans.
by various investigators may be due to experimental de- Not all amphibians in either tropical or températe re-
sign—aquatic versus terrestrial test chambers, photope- gions have equally broad ranges of thermal tolerance; in
riod, starvation versus feeding—or intraspecific variation fact, some species in both regions have limited acclima-
in the animáis tested because of differences in size, ma- tory abilities. Such species are physiologically less plástic
turity, sex, or place or season of origin. because of a small gene pool, low heterozygosity, or much
Magnitude of acclimation.—It is generally assumed inbreeding (i.e., the total morphological and physiologicai
that amphibians living in regions of high temperatures variability is less than in wide-ranging species); thus, shoulc
tolérate higher temperatures than those living in cooler local climatic conditions change, these species are likely
regions. Comparison of critical thermal máxima of trop- to become extínct. For example, Brattstrom (1970) founc
ical and températe species shows that amphibians living that two species of anurans (Kyarranus sphagnicola anc
in the tropics typically have higher critical or lethal tem- Philoría /rostí) living on mountaintops in eastern Aus-
peratures than ones living in the températe zones (G. tralia, where there is little environmental fluctuation, have
Snyder and Weathers, 1975), but amphibians from both essentially no ability to undergo thermal acclimatior.
regions are similar in their abiliües to undergo acclimation Likewise, Bu/o exsuí, restricted to one small valley ir.
to high temperatures (Table 8-2). In both regions the California, has limited temperature tolerances in com-
upper thermal tolerances of amphibians increase within parison with its wide-ranging relaüve B. bóreas. Centrc-
certain limits of thermal acclimation, as shown for various lenella fleischmanni in montane forests in Costa Rica has
 Relationships with the Environment
i .ery limited ability to adjust to changing temperatures tolerance responses to an altered thermal environment. 213
Erartstrom, 1968). Microhabitat temperatures may differ An organism might thus change its heat resistance with-
—ri-;derably from general ambient temperatures, as in out necessarily modifying its cold tolerance, or vice versa.
r¿ case of the interiore of bromeliads and banana plants Factors affecting thermal acclimation.—Differences
r-.abited by various anurans and bolitoglossine sala- in the magnitude of thermal acclimation in wide-ranging
randers in the Neotropics (Peder, 1982b). species have been noted already; no evident trends seem
Limited data on salamanders (V. Hutchinson, 1961) to be apparent in rates of acclimation by individuáis of a
irc anurans (Brattstrom, 1968, 1970; G. Zug and P. given species from different geographic regions. Limited
I_5. 1979) show that in species with broad geographical data suggest seasonal differences in magnitude and rates
tsxjes, especially laütudinally, there is geographic vari- of thermal acclimation in two salamanders, Notophthal-
••on in temperature tolerance; altitudinal effects corre- mus viridescens (V. Hutchinson, 1961) and Eurycea bis-
are nding to latitudinal gradients have been demonstrated lineata (Fig. 8-14; Layne and Claussen, 1982).
r 3ufo bóreas (Brattstrom, 1968) and Pseudacrís tri- Size possibly affects the critical thermal máximum. V.
cota (K. Miller and Packard, 1977). Hutchinson (1961), Gatz (1973), and Claussen (1977)
Only a few investigations on temperature tolerances found no significant intraspecific size effect in various kinds
•ave been concerned with critical minimum tempera- of salamanders, ñor did Heatwole et al. (1965) with two
xres. Brattstrom (1968, 1970) provided data on mini- species of frogs of the genus E/eutherodacty/us. How-
trum lethal temperatures for many kinds of anurans and ever, Sealander and B. West (1969) found a slight, al-
—r.cluded that high-tatitude species are more cold-tol- though insignificant, tendency for smaller individuáis of
ir^nt than tropical species (Fig. 8-13). species of salamanders to be more resistant to temper-
Rotes of acclimation.—Acclimation rates are highly ature than larger conspecifics, and Seibel (1970) found
-añable but usually follow a hyperbolic curve (Fig. 8-12). that larger individuáis of Rana pipieos have higher critical
~-.ere seems to be no correlation with laütude or altitude. thermal máxima than smaller conspecifics. In larval am-
Kowever, Claussen (1977) suggested that there is a cor- phibians, younger individuáis usually have greater heat
:=.ation between the magnitude and rate of thermal ac- resistance and broader ranges of tolerance than older
omation. He proposed an acclimation response ratio of larvae. Recently hatched larvae of Ambystoma macu/a-
ARR = ACTM/ZT as being the change in the critical tum and Taricha riuu/aris either do not respond to tem-
firmal máximum (ACTM) per degree Celsius change in perature differences, except extremes, or have notably
aiclimation temperature (AT). Because this ratio assumes slower responses than older larvae (P. Licht and A. Brown,
í linear relationship between the critical thermal maxi- 1967; Keen and Schroeder, 1975). The latter authors
—um and the acclimation temperature and because ac- found that among the larvae of three species of Ambys-
rimation rates usually follow a hyperbolic curve, Claus-
sén suggested using the time required for 50% acclimation
. 2AT). Acclimation is quite rapid (1/2AT of 2 days or
iess in most species), yet highly variable in magnitude
Table 8-3). Calculated acclimation response ratios in sal-
amanders vary from 0.12 for Desmognathus /uscus to 10.0-7.5-
I 19 for Cryptobmnchus alleganiensis and Necturus ma-
zjlosus; ratios have a broader range in anurans—from S7.5-5XW
<0.01 for Philoría /rostí to 0.40 for Scaphiopus hol-
srookii, Cydorana brevipes, Hyla cadaverina, and ñaña 152.5-5.0H
rcmitans (Claussen, 1977).
Although ACTM valúes for acclimation to lower tem- 12.5- 0.0-
peratures are similar to valúes for acclimation to higher
Bmperatures (Table 8-3; Figs. 8-12, 8-14), reverse ac-
i-nation is markedly slower in some species (e.g., No- 0.0- -1.0-
•jcchthalrnus viridescens, Chiropterotriton mu/tidentattis, below
ar.d Eurycea bislineata) and slightly faster in the large -1.0
acuatic salamanders, Cryptobranchus alleganiensis and
60 70
Necturus maculosus. Acclimation to máximum and min-
mum temperatures seems to be decoupled in magnitude Latitude of
35 well as in rate. Consequently, a considerable degree Most Northern Occurrence
oí independence seems to exist between the acclimation Figure 8-13. Relationship between cold lethal temperatures (50%
30 critical thermal máxima and critical thermal minima. survival) and latitude of northernmost occurrence of species of
anurans in North and Central America. Symbols are means of
As noted by Layne and Claussen (1982), this may have temperatures for a given species at a given latitude. Redrawn from
adaptive valué in allowing differential heat- versus cold- Brattstrom (1968).
ECOLOGY
214 toma, temperature selection is positively correlated with rehydratíon (Fig. 8-6). Dehydraüon decreases the critical
size and acclimaüon histories. On the other hand, the thermal máximum of juvenile Ambysfoma macu/atum
thermal responses of larval T. rívularís are similar to those (Pough and R. Wilson, 1970) and adults of A. jefferson-
of the adults (P. Licht and A. Brown, 1967), the mag- ianum and A. tigrinum (Claussen, 1977). On the con-
nitude and rates of acclimaüon of larval A. tigrinum par- trary, V. Hutchinson (1961) and Peder and Pough (1975)
allel those of adults (Nietfeldt et al., 1980). found that dehydration increased thermal tolerance in
The available data on the effect of water balance on Notophthalmus uiridescens. The. negative influence of
thermal acclimaüon are equivocal, although temperature dehydration on critical thermal máxima of Ambysíoma
acclimatíon has an effect on rates of dehydration and does not support the free-radical hypothesis advocated

Table 8-3. Rate and Magnitude of Thermal Acclimatíon ¡n Amphibians*

Initial Final AT V4AT ACTM

Species temperature (°C) temperature (°C) (°C) (Days) (°C) ACTM/AT ACTM/M¡AT
Salamanders
Cnjptobranchus alleganiensis 5 25 20 2.80 4.30 0.20 1.44
Cnjptobranchus alleganiensis 25 5 -20 2.15 4.52 0.23 2.10
Necturus maculosus 5 25 20 1.54 4.16 0.21 2.70
Necturus maculosus 25 5 -20 1.18 -3.20 0.16 -2.71
Notophthalmus uiridescens 4 20 16 0.17 2.53 0.16 9.37
Notophthalmus uiridescens 2C 4 -16 2.24 -2.78 0.17 1.24
Ambysíoma jeffersonianum 5 25 20 0.57 1.47 0.07 2.58
Chiropíeroiriíon mu/tidentatus 5 20 15 0.39 2.56 0.17 6.56
Chiropterotriton multidentatus 2C 5 -15 1.00 -2.89 0.19 2.89
Eurycea bislineata (spring) 5 25 20 0.12 1.37 0.07 11.42
Eurycea bislineata (summer) 5 25 20 0.60 2.27 0.11 3.78
Anurans
Scaphiopus holbrooki 5 23 18 0.69 7.92 0.44 11.48
Pseudophryne bibronü 5 25 20 0.27 6.44 0.32 23.85
Bufo americanus 1C 30 20 1.20 1.87 0.09 1.56
Bu/o debilis 5 23 18 1.42 4.71 0.26 3.32
Bu/o marinus 5 23 18 2.10 3.46 0.19 1.65
Bu/o ujoodhousü 5 23 18 0.08 2.86 0.16 35.75
Hy/a cadauerina 5 30 25 1.39 10.73 0.43 7.72
Liíoria eujingi 1C 20 10 1.42 3.13 0.31 2.20
Rana catesbeiana 5 23 18 0.12 2.00 0.11 16.67
Rana c/amiíans 5 23 18 2.17 7.82 0.43 3.60
Rana palustris 5 23 18 2.50 2.70 0.15 1.08
Rana pipiens 5 7 2 0.82 0.64 0.32 0.78
Rana pipiens 5 12 7 0.40 2.65 0.38 6.63
Rana pipiens 5 23 18 0.35 3.48 0.19 9.94
Rana pipiens 5 29 24 0.18 4.26 0.18 23.67
Rana pipiens 15 25 10 1.75 2.20 0.22 1.26
Rana pipiens 23 5 -18 0.43 -3.79 0.21 -8.81
*Based on Claussen (1977) and Layne and Claussen (1982).

CTMm CTMax _
CJ
*&***
<D +2- *o" -37 1^
<J ¿^'^'^
c
CD oó-s
y >^ r>
-
-36 r
Figure 8-14. Comparison of rates of o °//* / D"- _g o
thermal acclimation in the Q_ 'w / Sr^Q—- • „£- *~

salamander Eurycea bislineata at £ f / f ** 1

different seasons following transfer 3 i/ ' —
from 5 to 25°C. Open symbols 2 -1 - i / -34 I
connected by broken lines are means Q^ 1 =
for six individuáis collected in April; E ó / —
solid symbols connected by £> "2- • -33 ¿
continuous lines are means for seven
individuáis collected in August.
\dapted from Layne and Claussen 0 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7
1982). Days
 Relationships with the Environment
215
«*
:v Peder and Pough (1975) as a control mechanism of
r.ermal acclimation.
Photoperiod has an effect on thermal acclimation in
<J
iome amphibians, at least in some heliothermic anurans. 30-
Brattstrom (1968) determined that Bu/o bóreas, espe- O> o
D
rally toads that had been acclimated at higher temper- CO o
atures, modified their critica! thermal máximum in re- £25
H»nse to 8 and 16 hours of light. Comparisons of Hyla o
cfaia/is and Rana pipiens revealed significant variation in o A
A
tve critical thermal máximum over a 24-hour period in A A
AA
r. labialis acclimated at 25°C, light:dark (LD) 12:12, and £20 A
I pipiens at 25°C, LD 8:16, and at 15°C, LD 12:12
Mahoney and V. Hutchinson, 1969). In both of these
gpecies, times of highest thermal tolerance are in the late
—oming and early afternoon, and lowest tolerance is dur- 10 12 14
r<g the dark period; this 24-hour rhythm of tolerance is Time (MDT)
rcnsistent with the basking habits, which would expose Figure 8-15. Relationships of body temperature to time of day ín
frogs to the highest temperatures at about midday. Bufo debilis while basking (solid circles), hopping in sun (open
circles), and sitting in shade (triangles). Redrawn from Seymour
of the seasonal variation in critical thermal máxima (1972).
Notophthalmus viridescens may be controlled by
rrotoperiod. V. Hutchinson (1961) found that if these
rsewts were maintained on a 7-hour photoperiod cen- tween themselves and the environment. This was shown
tered on noon, the critical thermal máxima were signifi- for Acris crepitans and Rana pipiens by Brattstrom (1963).
antly lower than for those kept in constant light or con- Lillywhite (1970) found that bullfrogs, R. catesbeiana,
sant dark. Obviously, the interaction between light and thermoregulate behaviorally not only by changing loca-
Emperature in controlling biological rhythms is complex tions but also by altering their posture. Bullfrogs can re-
sr.d poorly understood. main exposed to insolaüon all day as long as a source of
moisture is available. Evaporative cooling, augmented by
Thertnoregulation postural changes and periodic rewetting of the skin, serves
As emphasized by Brattstrom (1979), the study of tem- to stabilize the body temperature at levéis lower than
Derature regulation in amphibians is complicated by the would be possible without the evaporative mechanism,
rsquirement of amphibians to maintain a moist skin. and enables these frogs to remain relatívely statíonary for
Tnermoregulation may be compromised by demands of periods under radiant heat loads that otherwise would
¿ater economy, whereas in other situations thermoregu- be lethal (see following section: Physiological Thermo-
arory demands may predomínate. regulation).
Seymour (1972) found distinct differences in body
E í havioral Thermoregulation. Field and laboratory temperatures of basking individuáis of toads, Bu/o de-
srjdies have provided sufficient Information to demón- bi/is, and those that were hopping in sunlight or sitting in
strate that at least some species of amphibians exert be- the shade (Fig. 8-15); mean body temperatures were
-javioral control over their body temperatures within the 30.9, 25.8, and 19.5°C, respectively. These toads also
tange of ambient temperatures available to them and in selected slopes that exposed them to the most direct in-
5ome cases actually exceed ambient temperatures. Ex- sola tion, and during the day moved from one slope to
oosure of amphibians to thermal gradients in the labo- another in response to the direction of insolaüon; body
ratory shows that individuáis select temperatures by mov- temperatures of toads basking on slopes facing toward
r.g to preferred parts of the gradient. This has been the sun were significantly higher than those of toads on
remonstrated most effectively in plethodontid salaman- the level or on slopes facing away from the sun
isrs (Spotila, 1972; Peder, 1982b) and in Ambystoma (means = 32.6 versus 29.5°C). Seymour (1972) sug-
^rvae (Keen and Schroeder, 1975). In the latter study, gested that in view of the lower body temperatures of
~ was shown that selection was accomplished by recur- toads hopping in the sun, the choice of basking sites
rent avoidance reactions, as in Taricha riuu/aris (P. Licht minimized convective and evaporative heat losses. Lilly-
nd A. Brown, 1967). However, in Ambystoma larvae, white (1970) noted that Rana catesbeiana hold the ven-
ríe accuracy with which body temperature is maintained tral surface off the ground when they are heat-stressed,
s less than that in juvenile Rana catesbeiana reported by which increases evaporative cooling vía convection, and
Lillywhite (1971b). lie prostrate under cool conditions.
Behavioral thermoregulation in diurnal anurans usually Many amphibians living at high altitudes increase their
nvolves moving into or out of sunlight or water, thereby body temperatures by exposure to insolation. Ambys-
changing the magnitude and direction of heat flux be- toma tigrinum in ponds at high elevations in the Rocky
ECOLOGY
216
Hyla labialis Atelopus ignescens
28-
-23
o 26-
§
-21 0>
3
o
224- o ro
o> -19 |
o.
,®
?22-\
Figure 8-16. Body temperatures of -17.
«b c
basking frogs in relation to ambient OD CE
I
temperatures (air temperatures in 20- o
shade 5 mm above ground for Hyla o -15
labialis; substrate temperature at site
of frog for Atelopus ignescens).
Diagonal lines connect isothermal 18- Oí
points. Data for H. labialis from -13
Valdivieso and Tamsitt (1974); data
for A. ignescens collected by W. E. 12 14 16 18 20 12 14 16 18 20
Duellman and L. Trueb. Ambient Temperature (°C)

Mountains move into shallow water on sunny days; at

night they retreat to the depths of the ponds, where the
water is warmer than that at the surface being cooled by 34
the night air (Heath, 1975). Basking behavior has been
reported for several anurans that live in températe re- u
gions (Brattstrom, 1963). Additionally, basking behavior 32-
0)
has been reported in two montane hylid frogs; Plectro- D
hyla glandulosa basks on rocks in and along streams in £ 30-
the mountains of Guatemala (Duellman, 1970), and the 0)
CL
Andean Hy/a labialis basks on the ground or on bushes E
(Valdivieso and Tamsitt, 1974). Neither species seems to 28-
employ postural modifications with respect to insolatíon.
Basking H. labialis elévate their body temperatures well
above the ambient temperature (Fig. 8-16). The high 26-
Andean Bufo spinulosus basks and actively moves about
during the day and seeks shelter when insolatíon ceases 2 4 6 8 10 12 14 16 18 20 22 24
(O. Pearson and Bradford, 1976).
Bufonids of the genus Atelopus are diurnal, and at least Time (hr)
some high montane species (A. ebanoides, ignescens,
Figure 8-17. Daily temperature regime of unrestrained Bu/o
and oxyrhynchus) bask. Duellman and Trueb's obser- marinas. Gíreles are mean body temperatures of one to four
vations on A. ignescens in the paramos of Ecuador show individuáis; dorted line = mean air temperature; solid Une = mean
that on bright sunlit days after rains, great numbers of substrate temperature. Redrawn from G. Zug and P. Zug (1979).
these frogs move about; subsequently individuáis remain
statíonary, usually in the sun on lee sides of clumps of
bunch grass, where they are exposed to insolatíon and tures than do large crevices or the interiors of the loes
protected from cold winds. These black frogs are able to (Peder, 1982b).
raise their body temperatures rapidly; within half an hour The body temperatures of nocturnal amphibians co-
after emergence, 20 individuáis had body temperatures incide closely with the ambient temperatures during pe-
of 0.5 to 4.6°C (mean = 1.45°C) above the temperature riods of activity. In these animáis, regulation of body terr-
of the adjacent substrate (Fig. 8-16). perature, if it occurs at all, is restricted to those times
Probably many kinds of high-altitude amphibians seek when the animal is in its diurnal retreat. The daily fluc-
shelters that have higher temperatures than surrounding tuatíon of body temperature of Bufo marinus is less thar.
áreas. This has been demonstrated for the diminutive that of the ambient temperatures (Fig. 8-17); during the
plethodontíd salamander Thorius narísovalis. These sal- night the body temperature is nearly equivalent to thz:
amanders select the smallest possible crevices under the of the ambient temperature, but during the day boc.
bark on logs; these small crevices have higher tempera- temperature remains well below ambient temperature (G
 Relatíonships with the Environment
lug and P. Zug, 1979). The lower temperature is the creased rates of digestión result in the depositíon of more 217
result of evaporative cooling of the body surface. fat, which is essential for survival during long periods of
dormancy.
- hysiological Thermoregulation. It is evident that
Aere is an interplay between behavioral thermoregula-
ton and water balance, but there has been only one in- GAS EXCHANGE
depth investigation of the mechanisms. In a study of the With the possible exception of cloacal tissues, amphibians
riermal parameters associated with evaporative water loss utilize every type of respiratory gas exchange known in
ii the bullfrog, Rana catesbeiana, Lillywhite (1971a) found vertebrales—gills, lungs, skin, and buccopharyngeal. Adults
r;at the periodic and synchronous discharge of the cu- of most kinds of amphibians, whether they be caecilians,
aneous mucous glands onto the integumentary surface salamanders, or anurans, use skin, lung, and bucco-
Dccurs in response to sympathetic nervous stimulation. pharyngeal respiration, but the lungless salamanders of
Tne frequency of discharge depends on central nervous the family Plethodontidae use only buccopharyngeal and
impulses and increases with higher temperatures. Exper- cutaneous gas exchange. Gills are common in the larval
mental results implicate the anterior hypothalamus in the stages of most amphibians and cease to function at meta-
:ontrol of the actívity of the mucous glands; apparently morphosis, but in some neotenic salamanders gilí respi-
r«eripheral afferents modify central impulses determining ration is retained in the adults.
ríe frequency of discharge. Thermal modulation of mu- Since the reviews of amphibian respiration by Foxon
rous discharge seems to function to maintain a moist (1964) and by Chugunov and Kispoev (1973), much
and therefore permeable) integument during terrestrial new information has become available that provides a
basking, thereby stabilizing body temperature. A slow rate basis for the interpretation of patterns of respiration dis-
of discharge results in drier (and less permeable) integu- played by amphibians. However, too littíe is known about
ment, so that at lower temperatures evaporative cooling the details of the morphology of respiratory structures,
s minimized. and even less is known about their functíons in all but a
This type of mechanism allows amphibians to raise few species.
rieir body temperatures by basking and to control the
body temperature by evaporative cooling. Obviously, such Gas Transportation
a mechanism is associated with diurnal basking and is an The exchange of gases between an amphibian and its
=daptation for cooling the body. There are no known environment is dependent on several structural fea-
physiological mechanisms by which an amphibian can tures—respiratory surfaces, circulatory system, and prop-
Lncrease its body temperature. Brattstrom (1970) sug- erties of the blood.
gested that basking Australian hylids, Litaría caerulea,
may have some control over the rate of water loss through Respiratory Surfaces. The contribution of each of
±e skin, thereby allowing this anuran to control the rate the four kinds of respiratory surfaces to total gas ex-
of evaporación and henee maintain a sublethal body tem- change depends on the organism's structure, stage of Ufe
perature under otherwise lethal conditions. history, and habitat, as well as environmental variables,
especially temperature.
Significance of Thermoregulation. In contrast to Cutaneous gas exchange is highly importan! in all ac-
reptiles in which basking (and therefore attainment of tive (as contrasted with resting or dormant) amphibians
preferred body temperature) commonly is a prelude to and may account for more than 90% of the exchange in
roraging activity, the reverse seems to be true in am- the lungless plethodontid salamanders, whereas in anu-
phibians, most of which have relatively broad ranges of rans and other salamanders the lungs account for varying
•Jiermal activity. Lillywhite et al. (1973) found that when amounts of the total gas exchange (Table 8-4). With in-
•uvenile Bu/o bóreas are well fed, they prefer tempera- creasing temperatures, the lungs and buccopharyngeal
tures of 26 to 27°C, but in the absence of food, they mucosa play an increasing role in oxygen uptake (see
prefer temperatures of 15 to 20°C. Peder (1982b) noted section: Factors Affecting Gas Exchange). Because oxy-
that subsequent to feeding, plethodontid salamanders gen uptake through the skin or gills is passive, it is de-
t.Pseudoeurycea smithi) had preferred body temperatures pendent on the proximity of capillaries to the surface,
of 3 to 5°C greater than those of unfed salamanders. density of capillaries, blood flow through the capillaries,
These observations are corroborated by field observa- the affinity of the hemoglobin to oxygen, and in the case
tíons on Rana catesbeiana (Lillywhite, 1970), B. wood- of the skin a moist surface. Uptake of oxygen through
housii (Hadfield, 1966), and B. spinu/osus (O. Pearson the pulmonary and buccopharyngeal üssue is dependent
and Bradford, 1976). Three aspects of thermal metabo- on these same factors and also the depth and rate of
lism seem to be evident in relation to behavioral ther- breathing movements. Increased utilizatíon of the lungs
moregulation. (1) By increasing their body temperatures, in respiration can be correlated with lung size and com-
amphibians increase their digestive rales. (2) Increased plexity and with the tidal volume and breathing rates.
digestive rates maximize growth in juveniles. (3) In- Comparison of the vascularity of the different respi-
ECOLOGY
218 Table 8-4. Contributions of Different Respiratory Surfaces to Gas Exchange in Various Amphibians"
Oxygen6 Carbón dioxidec
Species Cutaneous Pulmonary Branchial Cutaneous Pulmonary Branchial
Salamanders
Necturus maculosus 30.4 8.4 61.2 31.6 8.5 59.9
Siren lacertina 33.1 61.6 5.3 53.9 27.7 18.4
Ambystoma maculatum 68.4 31.6 — 79.6 20.4 —
Taricha granulosa 49.4 50.6 — 86.8 13.2 —
Desmognathus quadramaculatus 9.7 90.3a 88.9 11. ld —
Anurans
Xenopus laeuis 58.5 41.5 — 90.3 9.7 —
Scaphiopus bombifrons 32.4 67.6 — 74.3 25.7 —
Eleutherodactytus portoricensis 23.2 76.8 — 80.3 19.7 —
Bufo bóreas 44.4 55.6 — 79.0 21.0 —
Hyla gratiosa 35.9 64.1 — 73.4 26.6 —
Rana pipiens 45.8 54.2 — 76.0 24.0 —
"Based on data in Guimond and V. Hutchinson (1976), V. Hutchinson et al. (1968), and Whitford and V. Hutchinson (1963, 1965).
'Percentages of total oxygen exchange at 15°C.
cPercentages of total carbón dioxide exchange at 15°C.
dBuccopharyngeal only.

Table 8-5. Percentages of Capillaries in Different Respiratory

Structures in Various Amphibians11 90-
Buccal
Group Skin cavity Lungs 80-
Salamanders
Siren intermedia13 38.7 0.9 58.1 70-
Amphiuma means 31.3 0.5 68.2
Salamandra salamandra 41.4 1.3 57.3
Triturus (3 species) 74.5 2.0 23.5 £60
Taricha granulosa 64.5 4.5 31.0
o
Notophthalmus viridescens 72.8 3.9 23.3 £50
Rhyacotriton olympicus 85.6 5.3 9.1 o
Dicamptodon ensatus
Ambystoma (2 species)
54.0
56.1
3.5
3.0
42.5
40.9
I 40-
Plethodontids (7 species) 93.2 6.8 —
Anurans 30-
Xenopus íaeuis 33.9 0.2 65.9 20 30 40 50 60 70 8O 9C
Leiope/ma hochstetteri 65.1 3.0 31.9
Bambino (2 species) 47.6 1.2 51.2 Percent of Total Respiratory Capillaries
Pelobates fuscus 48.3 2.4 49.3 Figure 8-18. Relationship of relative amounts of cutaneous
Bufo (5 species) 27.8 1.4 70.8 vascularization and cutaneous gas exchange in various amphibians
Hy/a arbórea 24.2 1.1 74.7 (see Tables 8-4 and 8-5). Solid circles are oxygen exchange;
Rana (3 species) 34.4 0.8 64.8 V = 21.7 + 0.72 X, r = 0.748 (P < 0.05). Open circles are carbón
dioxide exchange; Y = 74.0 + 0.169X, r = 0.241 (not significara.
"Summarized from Czopek (1962) and Foxon (1964). Outliers (1 = Taricha; 2 = Siren) not included in regression
bPlus 2.3% in gills. analyses.

ratory surfaces shows that the percentage of Capillaries in ative of increased need for water uptake. Nevertheless.
the buccal cavity is usually minute compared to those in there is a positíve correlation between the relative amouns
the skin or lungs (Table 8-5). Exceptions are the lungless of cutaneous oxygen uptake and cutaneous vascular.-
plethodontíd Salamanders and Rhyacotríton olympicus, zation, although no such correlation exists for the relative
a salamander that dwells in cold water. The skin of ter- amount of carbón dioxide exchange (Fig. 8-18).
restrial anurans is more vascularized, relative to the lungs, The lungs vary in size from very small in some am-
than that of aquatic or semiaquatíc anurans; this suggests phibians that dwell in cold water (e.g., the salamander
that pulmonary ventilation is more importan! in the aquatic Rhyacotríton o/ympicus and the leptodactylid frog Te-
and semiaquatíc anurans, but the high degree of integu- matobius culeus in Lake Titicaca in the high Andes) r
mentary vascularity in terrestrial anurans may be indic- large in most terrestrial anurans, ambystomatid salamar-
 Relationships with the Environment
ar.d neotenic salamanders, such as Siren and Am- of pulmonary air during the second phase of the next 219
u-c. that Uve in poorly oxygenated water (see Chap- ventilatíon cycle (Fig. 8-19). Pressure is maintained by
14 :or details of pulmonary structure). the elastic fibers and smooth muscles of the lungs. This
r-<£ ventilation of the lungs is accomplished by a force- basic respiratory mechanism is not very efficient, but it is
en: mechanism (de Jong and Gans, 1969). In ñaña characteristíc of all living amphibians. Even the lungless
Bsoeana, buccopulmonary venülation comprises three plethodontid salamanders may obtain up to 24% of their
es DÍ cyclic phenomena: (1) Oscillatory cycles consist oxygen through the buccal mucosa (Whitford and V.
r-yfimic raising and lowering of the buccal floor with Hutchinson, 1965). Anurans are locked into this respi-
: -¿res open; in this way fresh air is introduced into ratory mechanism, for it is an integral part of the vocal-
i rucea! cavity. (2) Venülatory cycles consist of opening ization mechanism (see Chapter 4).
: : :s:ng the glottis and nares and the renewal of pul-
- : - ---: air. (3) Inflation cycles consist of a series of ven- Circulatory System. Circulaüon of oxygenated and
y cycles interrupted by an apneic pause. This res- deoxygenated blood in amphibians is not completely
- -v: -. mechanism depends on the activity of a buccal sepárate because of mixing in the heart (see Chapter 3
pump, which determines pulmonary pressure; ele- for details of structure). Although there is some mixture
EC pulmonary pressure is responsible for the expulsión of the blood in the heart, differential blood pressure caused

c cressure

'«tNTILATION PHASES

-a-ik movement

\cstril movement
Glottis ^•CLOSEÜ

Nostrils

r low at glottis

Figure 8-19. Diagrammatic

representation of buccal pump
respiration in Rana catesbeíana
showing temporal relationships
among lung pressure, buccal
= low at nostrils pressure, nostril and flank
movements, and airflow. Adapted
from de Jong and Gans (1969).
ECOLOGY
220 by vasoconstriction of certain vessels helps to regúlate 57 to 75 torr, in venous blood 31 to 37 torr, and in mixed
the flow. For example, Xenopus íaeuis breathes aerially blood 40 torr. The different interpretations of patterns of
at the surface of the water and depends on cutaneous flow of oxygenated and deoxygenated blood in a lungless
respiration when below the surface; approximately 58% salamander as contrasted with that in anurans possibly
of ¡ts oxygen uptake is cutaneous under experimental are associated with lunglessness, or there may be a basic
conditions at 15°C (V. Hutchinson et al., 1968). Moni- difference between salamanders and anurans.
toring of respiratory cycles and circulation by Shelton
(1976) revealed that gas exchange occurs at a high rate Characteristics of Blood. Oxygen transport by the
in the lungs when the frog is using aerial ventilatíon, but blood depends on several hematological factors—num-
the rate decreases rapidly when it submerges. The amount ber and volume of red blood cells (erythrocytes), he-
of blood flowing to the lungs is related to the extent that matocrit (percent of blood that is red blood cells), hemo-
they are ventilated. When Xenopus is not breathing, globin contení, and pH of the blood. The affinity between
vasoconstriction of the lung vessels reduces blood flow oxygen and red blood cells vanes with environmenti
in the pulmonary artery to low levéis, so that patterns of factors, such as temperature and partial pressure of oxy-
blood flow and pressure in the arterial arches can be gen; the latter commonly is measured as P50 (50% satu-
interpreted in terms of the constantly changing vaso- ration of the red blood cells with oxygen).
motor state of the lung vessels. Shelton (1976) hypoth- Blood characteristics with respect to oxygen transpor-
esized that the selective distribution of blood leaving the tation are known for only a few amphibians (Table 8-6
heart is achieved by maintenance of more or less sepá- Surveys of amphibian bloods by Lenfant and Johansen
rate streams of oxygenated and deoxygenated blood; the (1967) and by Johansen and Lenfant (1972) show z
separation of mese streams is affected considerably by clear trend toward lower oxygen affinities in the bloocs
the degree of vasoconstriction of the lung vessels. of amphibians that rely mostly on their lungs as con-
Measurements of the relative amounts of oxygen and trasted with aquatic amphibians that accomplish oxyger
carbón dioxide in vessels entering and leaving the heart uptake by means of gills, skin, and buccopharyngeal mu-
in Bu/o paracnemis also indícate a physical separation of cosa.
oxygenated and deoxygenated blood (Johansen and Di- Activity also has an effect on blood characteristics.
tada, 1966). especially in the case of dormant versus resting or active
On the other hand, in a study of the lungless sala- animáis. In dormant spadefoot toads (Scaphiopusj, P^
mander, Desmognathus fuscus, Piiper et al. (1976) con- valúes are lower than in resting individuáis, but hemo-
cluded that arterial and venous blood probably are com- globin levéis and hematocrit are not significantly difieren^
pletely mixed in the heart. Of the cardiac output of 0.11 Seymour (1973c) suggested that hemoglobin may func-
' to 0.19 ml-mirvg body weight of this salamander, less tion mainly for oxygen storage during dormancy. How-
than 50% of the blood is directed to the skin, where gas ever, in cocooned Pyxicepha/us adspersus, hemoglobr
exchange occurs; the majority of the cardiac output is concentration and hematocrit increase significantly
directed to other tíssues and organs, where oxygen is compared with nondormant frogs, reflecting dehydra-
delivered. Partial pressures of oxygen in arterial blood is tional hemoconcentration (Loveridge and Withers, 1981.

Table 8-6. Characteristics of the Blood of Some Species of Amphibians0

RBC1" volume RBCb Hemoglobin Concentration RBCfe O2 capacity
[mi (100 mi volume [g/(100 mi [g/100 mi Hb content [mi 02/(100 P-..
Species blood)-1] (V?) blood)-1] (HBC)-1] (pg) mi blood)-1] (mmh:
Caecilians
Bou/engeru/a taitanus 40.0 588 10.3 25.7 151 14.00
Salamanders
Cryptobranchus alleganiensis 49.0 7,425 13.3 27.1 2,010 — 2C :
Necturus maculosus 21.4 10,070 4.6 21.4 2,160 6.26 i"
Amphiuma means 40.0 13,857 9.4 23.5 3,287 7.26 se :
Taricha granulosa 36.7 3,336 9.5 13.2 837 9.70 36.5
Dicamptodon ensatus 24.2 4,938 4.4 15.6 880 5.60 31.6
Anurans
Telmatobius cu/eus 27.9 394 8.1 28.1 281 8.02 15.6
Rana catesbeiana 29.3 670 7.8 26.9 179 10.43 49.S
Rana esculenta 27.3 659 7.8 28.9 187 39.7
Rana pipiens 24.6 768 6.7 27.2 208 11.70 —
"Data from S. Wood et al. (1975) and V. Hutchinson et al. (1976).
bRBC = red blood count.
 Relationships with the Environment
Factors Affecting Gas Exchange 331
Respiratory rates, principally oxygen consumption, vary
with properües of the animáis (activity, surface área, and
body size) and environmental variables (temperature, .12-
oxygen pressure, moisture, and photoperiod).

Body Size and Surface Área. As expected, larger

amphibians consume more oxygen than smaller ones, -C g>
but the rate of oxygen consumption has a negative cur- CD
vilinear relationship with body size, at least in anurans
(Fig. 8-20). V. Hutchinson et al. (1968) concluded that •g o
the lungs are the most important respiratory structures in .06-1
anurans and that, in general, there is an inverse relation-
ship between body size and ventilatory rate and a direct
relationship between tidal volume and weight. The lungs
also are the most important respiratory structures in adult .03-
caecilians (A. Bennett and M. Wake, 1974). 20 40 60 80 100 120
In salamanders the respiratory surface área differs be- Rate of Oxygen Consumption (ml-g"1 hr1)
tween lunged and lungless salamanders; at weights of
more than 0.44 g, lunged salamanders have greater res- Figure 8-20. Relationship between body weight and rate of
oxygen consumption in 20 species of anurans at 15°C. Based on
piratory surface áreas than lungless salamanders of the data in V. Hutchinson (1971).
same weight (Ultsch, 1974), and this discrepancy in-
creases with body size (Whitford and V. Hutchinson, 1967).
The expected differences between lunged and lungless 160-
salamanders in rates of oxygen consumption are evident
in salamanders in hypoxic or aquatic media (Becken-
Températe Amphibians
back, 1975; Ultsch, 1976). In atmospheric air the rate of
oxygen consumption is similar for resüng lunged and
lungless salamanders under standard conditions (Peder, 3120-
1976). However, the reduced respiratory surface área in
large lungless salamanders apparently results in reduced g
capacity for oxygen exchange at postactívity times com- o.
E
pared to lunged salamanders (Peder, 1977; Withers, 1980).

Temperature. The effects of temperature on respira- 8 80-

C
üon were reviewed by Whitford (1973), who concluded oí
that in températe zone amphibians, except plethodontid
salamanders, pulmonary oxygen uptake increases with I
temperature and that tropical anurans have a rate of oxy- "o
gen consumption equivalen! to that of températe am- S 40-
phibians at temperatures of 10°C or more. In plethodon-
tid salamanders the rate of cutaneous gas exchange
increases with temperature, and aquatic salamanders have Aquatic Salamanders
a lower rate of oxygen consumption than other tempér-
ate amphibians (Fig. 8-21). —i—
The rates of oxygen consumption in relation to tem- 15 25
perature in plethodontid salamanders apparently are the Temperature (°C)
result of decreased respiratory surface área (absence of
Figure 8-21. Effect of temperature on rate of oxygen consumption
lungs). The lower rates in tropical anurans, relative to in varíous groups of amphibians. Redrawn from Whitford (1973).
températe anurans and lunged terrestrial salamanders,
indícate lower resting metabolic rates in tropical anurans
(Weathers and G. Snyder, 1977), a conclusión also Peder (1978a, 1982a) summarized existing data on
reached by Peder (1978b) regarding tropical versus tem- acclimation of amphibians. Acclimation temperatures al-
pérate plethodontids. These correlations suggest that tered standard metabolic rates of two températe zone
tropical anurans and plethodontid salamanders not only salamanders (Batrachoseps attenuatus and Tarícha to-
have lower metabolic rates but should have less capacity rosa) but not of two tropical salamanders (Bo/itog/ossa
for thermal acclimation of metabolism. occidenía/is and Pseudoeurycea smithi). Also, acclima-
ECOLOGY
222
¿;.

Figure 8-22. Aquatic leptodactylid

frog Atelognathus patagónicas from
Laguna Blanca, Argentina, 1275 m
elevation. The extensive flaps of skin
provide a greatly increased surface
área for respiration in cold water.
Photo by W. E. Duellman.

tíon temperature had a greater effect on several measures so as to break up the boundary layer between the water
of postactivity oxygen consumptíon in the températe zone and skin, thereby ventilatíng the cutaneous surfaces. This
species than in the tropical species. Investigations on habit also is characteristic of C. alleganiensis (Guimond
tropical and températe anurans have provided similar re- and V. Hutchinson, 1973).
sults; all températe zone species show significant accli- Oxygen transport characteristícs in Te/maíobius culeus
mation of metabolism, and all tropical species, except include the smallest erythrocyte volume known in am-
Rana erythraea, show no acclimation. Moreover, differ- phibians and the highest erythrocyte count and lowes:
ences in the abilities of tropical versus températe species P50 known for anurans. The oxygen capacity, hemoglo-
to undergo thermal acclimation of rates of oxygen con- bin concentratioh, and hematocrit valúes are higher than
sumptíon are contrary to the pattern for acclimation of in most amphibians. During a 10-week period of accli-
critical thermal máxima, in which tropical and températe mation from 3800 to 335 m, the erythrocyte count.
species show no consistent differences (Brattstrom, 1968; hemoglobin concentration, and hematocrit declinec
Peder, 1978a). steadily, thereby indicating that these characteristics are
subject to environmental influence. Comparable kinds of
Oxygen Pressure. Differentíal partial pressure of oxy- data on terrestrial amphibians from high elevaüons are
gen at different altitudes seems to be reflected in the lacking, so it is unknown if all of these characteristics oí
oxygen-carrying capacity of the blood. As early as 1951, T. culeus are associated strictly with lower oxygen pres-
Stuart noted that Bufo bocourti in the highlands of Gua- sure or with cold water.
temala had 22% more hemoglobin than B. marínus in
the lowlands. The only detailed work on a high altitude Moisture. The moisture coating the skin is importar.:
amphibian deals with the aquatic Te/matobius culeus, in diffusion. The only experimental data on the relation-
which lives in perpetually cold water (10°C) at an ele- ship of dehydration and oxygen consumption are from
vation of 3812 m in Lake Titicaca (V. Hutchinson et al., the Puerto Rican frog Eleutherodactylus caqui (Pough z
1976). This anuran has extensive flaps of skin that in- al., 1983). The metabolic rates of resting frogs increase
crease its surface área for greater cutaneous respiration, and the máximum metabolic rates decrease as the frocs
a condition also characteristic of some other inhabitants become more dehydrated.
of cold waters (e.g., Cryptobranchus alleganiensis and
Atelognathus patagón/cus; Fig. 8-22). In Telmatobius and Photoperiod and Seasonality. There are few daa
Cryptobranchus, at least, capillaries penétrate to the epi- on the effects of photoperiod on metabolic activity. 2=
dermis. When submerged in water with a low oxygen measured by oxygen consumption, and the experimenta
pressure, T. culeus periodically sways from side to side results and interpretaüons are ¡nconsistent (see review r.
 Relationships with the Environment
Turney and V. Hutchinson, 1974). Endogenous meta- Activity Levéis. Resting amphibians consume less 223
bolic rhythms were reported in températe but not tropical oxygen and therefore have lower metabolic rates than
amphibians; however, Weathers and G. Snyder (1977) active animáis (Fig. 8-23). Peder (1978b) demonstrated
demonstrated rhythmic metabolism in three species of these differences in 18 species of salamanders. Oxygen
tropical Rana subjected to different photoperiods. One consumption increases dramatically after short bursts of
aspect of rhythmic behavior that does seem to be ap- activity. Moreover, in lungless salamanders the rate of
parent is the increase in metabolism at times of normal máximum oxygen consumption is less than in lutiged
increase in activity in nature. F. Brown et al. (1955) re- salamanders, especially in larger salamanders and at higher
ported that amphibians have endogenous rhythms cor- temperatures. Few data are available on rates of oxygen
related with daily changes in ambient atmospheric pres- consumption in active versus resting anurans. Oxygen is
sure, but V. Hutchinson and Kohl (1971) found no such consumed at rates 3 to 10 times greater in active indi-
correlation in Bufo marinus. viduáis than in resting ones at the same temperature
Knowledge of seasonal variation in metabolic rates is (Seymour, 1973a; S. Hulmán and Withers, 1979). Pyxi-
very limited. Vernberg (1962) reported seasonal differ- cephalus adspersus is an excepüon in that the rate of
ences in the salamanders P/ethodon cinereus and Eury- oxygen consumption during activity is similar to that of
cea bislmeata; at 10°C the highest metabolic rates of both other anurans, but the rate at rest is much lower, about
species were in May and June, and the lowest were in 5% of that during activity (Loveridge and Withers, 1981).
October and November. Fitzpatrick and A. V. Brown There is a great reduction in metabolic rate in dormant
(1975) found that Desmognathus ochrophaeus have amphibians. Dormant Siren intermedia (Gehlbach et al,
adaptive pattems of partial metabolic compensation over 1973) and Scaphiopus couchn and S. mu/tip/icatus (Sey-
a range of seasonally encountered temperatures—i.e., mour, 1973b) consume oxygen at a rate equal to about
inverse metabolic compensation at a temperature com- 20% of that of resting individuáis, and Cyc/orana p/aty-
monly encountered during winter dormancy, and tem- cepha/a has a rate of about 30% of resting individuáis
perature-insensitíve acute metabolic rates during short- (van Buerden, 1980). In dormant and cocooned Pyxi-
term changes in temperatures similar to those encoun- cepha/us adspersus, the rate is equal to 16% of that of
tered during early spring and autumn. resting individuáis (Loveridge and Withers, 1981). There
Natural seasonal differences in metabolism, as measured is a corresponding decrease in heart rate in dormant am-
by rates of oxygen consumption, may reflect differences phibians.
in activity levéis (see following section), energy metabo- The mechanism by which the metabolic rate of dor-
lism, or reproductive effort, especially during vitelloge- mant amphibians is lowered to substantially less than the
nesis (see Chapter 2). Endogenous rhythms are evident standard metabolic rate is unknown. The low rate of oxy-
in reproductive cycles in températe and some tropical gen consumption of dormant Scaphiopus couchii is not
amphibians. Furthermore, as concluded by Lagerspetz associated with tissue acidosis (Withers, 1978), whereas
(1977), the seasonal variation of metabolism in amphib- the tissues of Pyxicepha/us adspersus are acidotic. This
ians is controlled largely by the central nervous system acidosis probably is associated with cocoon formation
with the thyroid and the autonomic nervous system as rather than with dormancy per se and is not responsible
principal mediators. for the decline in the rate of oxygen consumption that

Figure 8-23. Oxygen consumption before,

during, and after activity at 20°C by Hyla regula
(solid line), Batrachoseps attenuatus (broken
line), and Geotrypetes seraphini (dotted line).
Rest 10 20 30 40 50 The hatched vertical bar is a brief period of
activity stimulated by an eléctrica! current.
Time (min) Redrawn (rom A. Bennett and M. Wake (1974).
ECOLOGY
224 accompanies dormancy but precedes cocoorT formation genase) are twice as great in R. pipiens (primarily an-
(Loveridge and Withers, 1981). aerobic during activity) as in Bufo bóreas (primarily aerobic)
(A. Bennett, 1974). Species that rely on burst activity for
rapid escape utilize anaerobic metabolism. The more aer-
ENERGY METABOLISM obically competent amphibians are physiologically inca-
AND ENERGY BUDGETS pable of this rapid activity and rely on static defense
Energy production in amphibians has been reviewed by mechanisms (Taigen et al., 1982).
A. Bennett (1978) and Brattstrom (1979). Most studies on fatigue in amphibians have empha-
sized lactate removal with recovery. In Batrachoseps at-
Energy Metabolism tenuatus, Peder and L. Olsen (1978) noted that a major
The relative contributions made by aerobic and anaero- synchrony between recovery from fatigue and lactate re-
bio pathways to activity metabolism is dependen! on work moval occurs during the first 30 minutes after exhaustion,
output. At low-level sustainable locomotion, aerobic ca- and for the next 4.5 hours, recovery parallels lactate re-
tabolism of carbohydrates and fats probably accounts for moval. The relationships among oxygen concentration,
all of the work output. A certain amount of anaerobic recovery from fatigue, and lactate elimination suggest that
metabolism, causing a rise in blood láclate, may occur at oxygen debt is an important aspect in recovery from ex-
the initiation of exercise until oxygen supply systems catch haustion. Therefore, rates of postactivity oxygen con-
up with oxygen requirements. This iniüal anaerobiosis sumption may limit rates of recovery. There are intra-
makes little contribution to overall energetics if activity is specific size differences in rates of fatigue. For example,
prolonged and remains at a low level. As long as no juvenile toads, Bufo americanus, become exhausted much
lactate accumulates or is excreted, oxygen consumption more rapidly than adults (Taigen and Pough, 1981).
accounts for the total energy output. Lactate may be
formed in muscle or other tissue, may enter the blood, Energy Budgets
and be catabolized aerobically elsewhere. There are few studies on the energy budgets of amphib-
In general, aerobically supported metabolism functions ians. Fitzpatrick (1973b) studied energy budgets in Eu-
at low rates of locomotion; mis is supplemented by an- rycea bislineata, and G. Smith (1976) produced an en-
aerobic metabolism during burst speeds. However, am- ergy budget for Bufo terrestrís. Assuming a digestive
phibians cannot sustain burst speed for more than 1 or assimilation efficiency of 74% for that species, approxi-
2 minutes, after which they become fatigued and unre- mately half of that energy goes into metabolic costs and
sponsive. Burst activity is fueled mainly, or almost exclu- half into production (Fig. 8-24). The amount of energy
sively, by anaerobic metabolism. During 2 minutes of devoted to reproduction will depend on the age and sex
activity, lactic acid formation accounts for two-thirds or of the toad and on the season of the year.
more of the total adenenosine triphosphate production In terms of energy metabolism, and thus costs of vari-
(A. Bennett and P. Licht, 1973). Because of the large ous functions, it is important to know how amphibians
and rapidly mobilized anaerobic potential and the relative partition the utilization of energy seasonally. Lillywhite e:
low levéis of oxygen consumption, burst activity is es- al. (1973) suggested that behavioral thermoregulation and
sentially oxygen-independent. The temperature inde- energy partitioning in juvenile toads, Bufo bóreas, max-
pendence of lactate formation in comparison with aerobic imize growth, thereby shortening the time to reach adu>.
scope (A. Bennett and P. Licht, 1974) provides the func- size. Also, many kinds of amphibians must accrue enero'.
tional basis for the temperature independence of burst reserves for survival of long periods of dormancy. In spe-
activity. The anaerobic metabolic mode exerts an even cies having a short period of activity because of brief rainy
greater influence on total metabolism at low body tem- seasons or brief summer temperatures, energy must be
peratures. Although recovery from activity requires much partitioned between reproduction and reserves.
more time at lower temperatures, anaerobic metabolism Marked seasonal changes occur in liver and musck
provides the capacity for rapid activity. glycogen, blood glucose, and body lipids in amphibians
Aerobic and anaerobic capacities of amphibians are living in seasonal environments. For example, Byrne an;
correlated inversely in various species (A. Bennett and R. J. White (1975) found that in Rana catesbeiana lipic
P. Licht, 1973; J. Baldwin et al., 1977; Harlow, 1978); reserves become exhausted from the time of emergenc¿
the total energy output during activity is similar but the through the breeding season. Lipid reserves increase prior
componen! factors are highly variable. For example, spe- to and into dormancy, whereas levéis of blood glucosa
cies having the greatest aerobic scopes (e.g., Taricha, rise during the breeding season and are lowest upor
Bufo, and Scaphiopus) do not produce large quantities emergence from dormancy. Presumably these levéis o:
of lactic acid during activity, whereas those that produce body composition are in response to seasonal enviro-.-
large amounts (e.g., Batrachoseps, Hyla, and Rana) have mental changes and associated activities on the pan c:
low aerobic scopes. These differences seem to have an the frogs. Seasonal changes in carbohydrate, protein nu-
enzymatic basis; reaction rates of two regulatory glyco- cleic acid, body lipid, and fat-body lipid levéis dunrc
tylic enzymes (phosphofructokinase and lactate dehydro- dormancy in Cyclorana platycephala indícate that fa:-
 Relationships with the Environment
body lipids provide most energy for larger individuáis (fat Environment = 100% 225
bodies account for up to 20% of the weight in large
individuáis), whereas smaller frogs have proportionately
smaller fat bodies and draw on other energy reserves
ivan Buerden, 1980). No comparable studies have been Ingestión
conducted on amphibians in aseasonal environments.

ECOLOGICAL SYNTHESIS Unassimulated Assimulated

The interrelationships of physiological mechanisms with Energy (26%) Energy (74%)
one another and with the environment are complex. With
the exceptíon of Tracy's (1975, 1976) model of moisrure
and temperature relationships for terrestrial amphibians,
no broad models of temperature-moisture-respiration- Metabolic Tissue
activity have been generated. Tracy's models do take into Costs(38%) Production (36%)
account that evaporative heat losses tend to offset radia-
tive heat gain in basking anurans, but basking anurans ... 1
may rest on substrates that are much warmer than the r~
valúes used in the model. Therefore, it is fairly easy for Reproduction (0-36%) Growth (0-36%)
an anuran to elévate its body temperature by basking.
However, Tracy suggests that amphibian thermoregula-
üon is crude or nonexistent because of the constraint of
evaporation on the rise in body temperature. In fact, this
effect actually facilitates thermoregulation. Fat — i— Lean Dry
Accumulation (5.4%) Biomass (30.6%)
Most efforts have been directed toward seeking cor-
relatíons between two variables, such as temperature ver-
sus rate of evaporative water loss, or temperature versus Figure 8-24. Energy budget of a toad, Bufo terrestris, weighing
33 g and maintained in the laboratory at 25°C. Broken lines
metabolic rate. The time is ripe for a multivariate ap- indícate feedback mechanisms. Adapted from G. Smith (1976).
proach to physiological responses. Unfortunately, com-
plete data sets for diverse taxa are not available. Fur-
thermore, differences in experimental design have resulted The ability to obtain moisture from soil having rela-
in noncomparable measurements. tively low water content and the ability to concéntrate
Until such analyses have been performed, precise pre- solutes (thereby increasing water uptake) and to store
dictions about the collective physiological responses of water in vesicles enable many kinds of amphibians to live
diverse amphibians to different environmental conditions in subhumid áreas. Thus, these physiological features are
are impossible. Nevertheless, based on the available data characteristic of desert inhabitants, such as Scaphiopus,
and correlations, it is possible to make some generaliza- Cychrana, and Bu/o. Furthermore, these attributes allow
tions about the ecological physiology of amphibians. these animáis to survive long periods of dormancy, dur-
The physiological attributes of animáis are among the ing which their metabolism is lowered and respiration is
principal factors that díctate how a species survives under primarily by ventilation of the lungs. In contrast, pletho-
a given set of environmental conditions, and therefore dontid salamanders have much lower capacities for water
influence the habitáis utilized and the activity patterns. In uptake from such soils, water storage, and solute con-
most cases it is not possible to pinpoint one physiological centrations, and the absence of lungs necessitates cuta-
mechanism that is responsible for the ecological limita- neous respiration; these characteristics preclude pletho-
tions of a particular species; instead, a combination of dontids from inhabiting xeric áreas, except where suitable
interacting mechanisms results in a suite of attributes that local microhabitats (e.g., spring seepages) exist. The ab-
adapt a species for existence under a set of environmen- sorption of water from soil probably is unique to am-
tal variables. phibians; no other vertebrales have this ability. The gen-
Moisture is the principal factor affecting the ecological eral impression that the permeable skin is a detriment to
distributions of amphibians. Rates of evaporative water survival in dry conditions is incorrect, for actually the
loss and water uptake from the environment must be permeable skin is an important factor in water uptake.
balanced with respect to activity. An amphibian may be Generally, amphibians that live in subhumid environ-
able to sustain considerable water loss during periods of ments are moderately large, have relatively short limbs,
activity if it can replenish water between these periods. If and therefore have relatively small surface-area/volume
the animal cannot tolérate much water loss, it can be ratios. These animáis have relatively low amounts of sur-
active only in áreas where, or at times when, ambient face área for evaporative water loss, and ventilation of
moisture content is high. the lungs is the primary means of gas exchange. Fur-
ECOLOGY
226 thermore, it seems that thesc animáis characteristically (e.g., Lepidobatrachus and Pyxicepha/us) with its attend-
have a high aerobio scope of metabolism allowing sus- ant modifications of water loss, osmoconcentration, and
tained low levéis of activity without building up an oxy- metabolism (Loveridge and Withers, 1981; McClanahan
gen debt. In contrast, small amphibians with relatively et al., 1983). Few amphibians can tolérate saline condi-
long limbs (and tails in salamanders) are inhabitants of tions, but osmoregulatory adaptations allow Rana can-
humid environments, where rates of evaporative water criuora to inhabit brackish water, where it has no other
loss are relatively low. Constant moisture on the skin anuran competitors (Cordón and Tucker, 1968). The ac-
allows for effective cutaneous respiration. In these ani- cumulation of glycerol in body tissues provides an anti-
máis, high anaerobio scopes of metabolism may be the freeze for some anurans, thereby allowing them to sur-
rule. vive subfreezing temperatures during hibernation (W.
The combinaüon of available moisture and ambient Schmid, 1982).
temperature may greatly restrict the distribution of some The diel and seasonal activities of amphibians are
species. Thermal tolerances of some montane species are regulated by environmental conditions, principally mois-
quite narrow, and these in combination with moisture ture and temperature. The interaction of these variables,
requirements presumably are the factors that restrict the especially as it affects condensation of moisture, is ex-
distributíons of such species to specific microhabitats within tremely important in the timing of diel activity by am-
limited geographical áreas. Other species have broad tol- phibians. For example, on rainless nights many nocturnal
erances to temperature and moisture and consequently bree frogs do not emerge from their diurnal retreats until
may have broad ecological and geographical distribu- the dew point has been reached and moisture condenses
tions. Perhaps the best example of a broadly tolerant on the leaves. Other arboreal frogs may emerge when
species of amphibian is Bu/o marinus, which lives in rain- the leaves are dry, but the frogs assume moisture-con-
forests and semideserts from sea level to elevations of serving postures and do not cali (Pough et al., 1983).
more than 2000 m. In at least some species that have The seasonal differences in temperature at high lati-
broad ecological tolerances, there are interpopulational tudes and in soil moisture at all latitudes have obvious
differences in physiological tolerances, for example, in limiting effects on amphibian activity, especially repro-
critical thermal máxima for example, in B. marinus (G. duction. Within this broad framework of seasonality, sub-
Zug and P. Zug, 1979), rate of evaporative water loss in tle differences in physiological tolerances can influence
B. arenarum (Cei, 1959), and rehydration rate in E/euf/i- the times of activity in different species. Thermal toler-
erodactylus caqui (van Berkum et al., 1982). ances of two species of salamanders and three of anurans
The local distributions of amphibians may be deter- in the northeastern United States are related to their times
mined by their tolerances of moisture or temperature. For of emergence and utilization of a breeding pond (Gatz.
example, the local distributions of two salamanders in the 1971). Of course, successful reproduction also depends
Appalachian Mountains seem to be the result of different on the physiological tolerances of the embryos (see Chapter
moisture requirements (R. Jaeger, 1971). Plethodon ci- 7).
nereus requires the moisture in the deep soils, whereas The inverse correlation of aerobic and anaerobic met-
P. ridimondi can tolérate the drier slopes. Water absorp- abolic scopes found in those few amphibians that have
tion rates in Puerto Rican frogs Eleutherodactylus antil- been examined may have broad ecological implications.
lensis and E. coqui seem to limit the distribution of the not only in escape behavior, as emphasized by A. Ben-
smaller E. antillensis as compared with the populations nett (1978), but also in habitat selection and foraging
of E. coqui that have larger body sizes (van Berkum et behavior. If burst activity is possible only in those species
al., 1982). Studies on four other Puerto Rican Eleuth- having high anaerobic scopes, it is most likely that tree
erodactylus (Pough et al, 1977) showed interspecific dif- frogs that leap from branch to branch will have high an-
ferences in microhabitats and activity patterns with re- aerobic scopes, as will amphibians that pursue their prey.
spect to rates of evaporative water loss, resistance to On the other hand, those that have slow, delibérate
desiccation, temperature selection, and critical thermal movements are expected to be primarily aerobic.
máxima. Behavioral thermoregulation probably is far more
Combinations of some physiological and behavioral common among amphibians than has been realized. The
mechanisms apparently have coevolved so as to permit subtle changes in temperature preferences among cryptic
the existence of some species in otherwise uninhabitable species and the more obvious differences among basking
environments. The most striking of these combinations species may be correlated with digestive efficiency. Be-
is that of lipid waterproofing, skin wiping, high osmocon- cause there is a direct correlation between temperature
centration, uricotelism, and quiescence exhibited by some and metabolic rates, digestión will be facilitated at higher
species of Phyllomedusa in and regions in South America temperatures. In the presence of an abundance of food.
(Shoemaker and McClanahan, 1975; Blaylock et al., rapid digestión permits increased rates of ingestión, and
1976). Prolonged survival in dormancy apparently is en- the resulting intake and assimilation of energy will result
hanced by formation of cocoons in burrowed anurans in increased rates of growth and/or accumulation of fats.
 Relationships with the Environment
Although there are definite physiological limitations evolved so that amphibians as a group are capable of 227
:r.aracteristic of amphibians, especially permeability of various kinds of actívities in diverse environments. Thus,
±e skin, absence of an internal thermoregulatory mech- we should not "pity the poor frog" as jested by Bratt-
anism, and incomplete segregation of oxygenated and strom (1979); instead, we should marvel at the diverse
reoxygenated blood, many physiological adaptations have physiological adaptations of amphibians.
 CHAPTER 9
T*>e different manners ofcapturing prey
accountfor such differences as
n the diet of adult frogs and

G. K. Noble (1931b)
Food and
Feeding

T he feeding strategies of amphibians include their

choice of prey and the ways in which they lócate, cap-
Prey-Capturing Mechanisms and Strategies. The limited
informatíon on amphibian diets indícales that all adult
ture, and ingest prey. Amphibians generally are consid- amphibians are carnivores; most feed principally on in-
sred to be feeding opportunists with their diets reflecting sects, although many species eat a wide variety of inver-
the availability of food of appropriate size. This may be tebrates.
true for some, but results of field and laboratory studies Herbivory is characteristic of anuran larvae, but it may
show that some species are selective in their feeding. occur in other amphibians; for example, the aquaüc sal-
Many constraints influence the diets and feeding habits amanders of the genus Siren have been reported to have
of amphibians, including extrinsic factors such as sea- large quantities of vegetable matter in their digestive tracts
sonal abundance of food and presence or absence of and to eat E/odea, as well as aquaüc invertebrates (Ultsch,
compeütors, and intrinsic factors such as ecological tol- 1973). Bufo marinus may eat vegetable scraps and canned
erances and morphological constraints that relate to on- dog food (Alexander, 1964; Tyler, 1976).
togenetic stage, size, and specializations. Ultimately, feed- Some anurans are especially voracious eaters. Large
ing must be efficient—i.e., more energy must be gained anurans, such as Cemtophrys ornato, Discodeles guppyi,
from the food than is expended in obtaining it, thereby Pyxicepha/us adspersus, and Rana catesbeiana, com-
maximizing energy gain. These factors, as they pertain to monly feed on large prey Ítems, such as small mammals,
adult amphibians, are discussed in this chapter. The food birds, turtles, snakes, and other anurans (Fig. 9-1). Dis-
and feeding of larval amphibians, especially tadpoles, are codeles, found in the Solomon Islands, eats land crabs
treated in Chapter 6, and the intraoviducal feeding by (Boulenger, 1884). W. Branch (1976) reported a Pyxi-
viviparous species is discussed in Chapter 5. cepha/us adspersus that had eaten 17 newly born cobras
(Hemachatus haemachatus) and another that had at-
tacked a young chicken. Some large salamanders also
PREY SELECTION capture relatívely large vertebrales; Dicamptodon ensaíus
Most accounts of amphibian feeding are anecdotal and eat plethodontid salamanders, frogs, snakes, mice, and
involve only a few taxa. Consequently, Me is known shrews (Bury, 1972). These prodigious gastronomic feats
about prey selection and foraging strategies; the latter are are exceptíons, as are the feeding on marine crabs by
discussed in the last section of this chapter: Evolution of Rana cancriuora (Elliott and Karunakaran, 1974), on ma-
229
ECOLOGY
230

Figure 9-1. A captive South African

bullfrog, Pyxicephulus adspersus,
engulfing a rat. Photo by W. E.
Duellman.

riñe invertebrates by the leptodactylid Thoropa miliaria gest increasingly larger prey Ítems as well as a broader
(Sazima, 1972), and on terrestrial gastropods by hyper- spectrum of prey sizes. Likewise, at least some terrestrii
oliid frogs of the genus Tomierella (Drewes, 1981). plethodotid salamanders show the same trends in in-
creasing the size, in addition to the diversity, of their pre.
Prey Availability among larger individuáis—e.g., Plethodon wehrlei (HaL
General availability of prey of the appropriate size and 1976) and Batrachoseps atienuatus (Maiorana, 1978).
type seems to be a basic constraint on th diets of am- An Ontogenetic shift in the size of prey selected by
phibians. For example, analyses of stomach contents of larval salamanders may be a function of developmenta.
five species of salamanders in New England (T. M. Bur- changes (e.g., increased number of teeth or increased
ton, 1976), Acris crepitóos in Indiana (Labanick, 1976), mobility) as well as increased gape (e.g., in postmeta-
and terrestrial eft stages of Notophhalmus viridescens in morphic anurans). Gape is known to be a factor in thé
New York (MacNamara, 1977) revealed that the abun- size of prey eaten by various species of anurans (Tori
dance of food Ítems in the stomachs was correlated with 1980a) and at least one salamander (R. L. White, 197"
the relative prey abundance in the habitat.
Habitat
Ontogenetic Changes Individuáis of a particular species may exhibit significare
As individuáis become larger, the kinds of prey that they differences in the kinds and amounts of prey eaten r
select may change. Ontogenetic changes in diets of larval different habitáis; this mainly reflects differences in pre.
salamanders were reported by Brophy (1980); as they availability among habitats. Thus, Inger and Marx (1961
grew, larvae of Ambystoma tigrinum and Notophthalmus found noticeable differences in stomach contents of sev-
viridescens increased their predation on snails and de- eral species of anurans at different elevations in the
creased their predation on smaller Ítems (ostracods and Upemba National Park in Zaire, and Barbault (1974) notec
cyclopoid copepods). In addition, there was a significant differences in diets of anurans in savanna and forest hab-
increase in the variety of prey taxa in larger Ambystoma itats in the Ivory Coast.
larvae. Larval Triturus uu/garis feed primarily on small Differences on a more local scale also are evident. Frr
zooplankton (chydorids, daphniids, and cyclopoid co- example, in freshwater habitats, the diet of Rana canc*--
pepods); as they grow and develop more teeth, the lar- vora consists mainly of insects, but in nearby bracios:
vae pursue and capture larger prey (principally chiron- water the frogs eat mostly crustaceans (Elliott and K~
omid larvae), although larger larvae do not select larger runakaran, 1974). Newts (Taricha granulosa) in a per-
individuáis of a given prey species (G. Bell, 1975). During manent pond eat a greater diversity of prey than do r-
postmetamorphic growth, hylid frogs (Acris crepitans, La- dividuals in a temporary pond (R. L. White, 1977
banick, 1976; Pseudacris tríseríata, Christian, 1982) in- Different diets of individuáis of the Argentine leptoda:-
 Food and Feeding
?.~¡id Pleurodema cinérea are correlated with terrestrial activity patterns, size of the prey species became an im- 231
ar.d aquatic feeding (Hulse, 1979). portant factor in prey selection, with the larger prey being
selected. Analysis of stomach contents of the Malaysian
Seasonality ranid Amolops larutensis, and activity patterns and abun-
Seasonal differences in diets have been reported for vari- dance of prey species throughout the year led Berry (1966)
nus species oí amphibians (e. g., Rana pretiosa, F. Turner, to conclude that diet selection by this frog is associated
1959; Notophthalmus uiridescens, T. M. Burlón, 1977; most closely with activity of the prey.
sr.d Plethodon glutinosus and P. jordani, Powers and
Tienen, 1974). Surveys of diets of many anurans in a
[ aeasonal tropical environment in West África revealed LOCATION OF PREY
-onceable differences throughout the year (Inger and Marx, Basically two kinds of foraging strategies are utilized by
1961). Among 13 species of anurans dwelling on the amphibians. Most anurans have adopted a sit-and-wait
iorest floor in Amazonian Perú, the diversity of food eat- strategy, whereas active foraging seems to be more com-
en by some species was greatest in the dry season (Toft, mon among some salamanders and apparently is char-
1980a). Moreover, a comparison of diets among forest- acteristíc of caecilians. However, the strategy used by an
5oor anurans at a drier site and a wetter site in Panamá individual may vary with the abundance of prey. The
rsvealed greater differences between sites than between method of monitoring prey abundance may depend on
5¿asons at any one site (Toft, 1980b). the sensory mechanism employed by the predator.
Seasonal differences in diets reflect availability of prey Predators using olfactory or tactile stimuli to detect prey
and, in some cases, seasonal differences in selectivity by may not be able to perceive either relative or absolute
mphibians (e.g., certain forest-floor anurans; Toft, 1980a). abundances of different kinds of prey without actually
This selectivity may be "forced" on the amphibians by capturing them. Conversely, encounter rates may be used
iactors other than food, especially by the necessity of more commonly by species that search for prey visually.
roraging under physiologically tolerable moisture condi-
tions. For example, the plethodontid salamander Des- Visual Detection
"lognathus /uscus demónstrales a selecüon for larger prey The vast majority of anurans and salamanders use visión
*-ith increased precipitation (Sites, 1978). Plethodon ci- in the final encounter with a prey item, although prelim-
lereus forages in moist leaf litter; when the leaf litter is inary location of prey also may involve other cues. Sev-
dry, the salamanders are confined to feeding on limited eral studies embracing field observations and laboratory
amounts and kinds of prey occurring under rocks or logs experiments indícate that visión is of primary importance
R. Jaeger, 1980). On foggy or rainy nights, P. cínereus in locating prey. This has been demonstrated for such
climbs on vegetation and feeds on kinds of insects not diverse salamanders as Salamandra (Luthardt and G. Roth,
presen! on the ground, actually ingesting more food than 1979), Trirurus (Margolis, 1976), Notophthalmus (J. Martin
conspecifics on the forest floor (R. Jaeger, 1978). et al., 1974), Ambystoma (Lindquist and M. Bachmann,
The seasonal activity of certain species is determined, 1982), Hydromantes (G. Roth, 1976), and Plethodon (R.
in part, by the activity of their prey. This is especially Jaeger et al., 1982), as well as various anuran species of
evident among prey specialists. The activity of the ter- the genera Bufo (Brower et al., 1960; Heatwole and
mite-eaüng anuran Breviceps verrucosus in South África Heatwole, 1968; Ewert, 1976; Borchersetal., 1978) and
:s timed to the swarming of termites (Poynton and Pritch- Rana (Maturana et al., 1960; Kramek, 1976).
ard, 1976). The period of feeding activity by the spade- Visual detection is most common in those species that
foot, Scaphiopus couchü, in southwestern North America have adopted a sit-and-wait strategy. Once a prey item
also is correlated with the swarming of termites (Dimmitt is sighted, it may be pursued for a short distance before
and Ruibal, 1980). capture. For example, the tree frog Hy/a cinérea obtains
Diel activity of prey may account for the predator's only 12% of its prey without pursuit; 88% of the prey
feeding activity and, therefore, kinds of prey taken. For Ítems are captured after visual detection and a short pur-
example, peak surface activity of three species of srre'am- suit (Freed, 1980).
side plethodontid salamanders is highly correlated with Recent experiments on the elicitaüon of feeding re-
the activity of potential prey at dusk or shortly after dark sponses in amphibians that use visual cues (Borchers et
(Holomuzki, 1980). Freed's (1980) analysis of prey be- al., 1978; G. Roth, 1978) indícate a complex inter-
havior and feeding selectivity by the tree frog Hy/a ci- relationship among stimulus parameters of velocity, size,
nérea suggested that the frogs selected prey in relation and orientation with respect to the direction of movement
to the proportion of time that the prey species was active of the prey. For example, in order to elicit maximal prey-
and the kind of activity displayed by the prey. Thus, catching behavior by Salamandra salamandra, it seems
increased frequency of prey activity resulted in a per- that stimuli of a certain orientation must move at a certain
ceived increase in the density of that prey species for the velocity and in a certain manner (Luthardt and G. Roth,
predator, thereby resulting in greater predation. When 1979). Elongation of the prey image along the axis of
prey selection was limited to prey types having similar movement facilitates prey capture by Bufo marínus; the
ECOLOGY
232 toad strikes mainly at the leading object when stimuli Bufo woodhousii were alerted to the presence of insects
travel orthogonally to the toad's opüc axis (Ingle and by the sounds they produced. R. Jaeger (1976) observed
McKinley, 1978). that B. marinus were attracted to calling frogs, Physalae-
Visual cues also can be important in identifying kinds mus pustutosus, which they consumed. Large carnivo-
of prey, such as those that may be optimal in energy rous anurans that prey on smaller anurans also may uti-
contení or that may be distasteful. Experiments with Bufo lize auditory cues to lócate prey.
terrestrís (Brower et al., 1960) revealed that the toads
learned to reject bumblebees (Bombas americanorum)
and their robberfly mimics (Mallophora bomboides) by CAPTURE OF PREY
sight alone. In addition to differences in kinds of prey and foraging
strategies, amphibians exhibit striking differences in feed-
Olfactory Detection ing mechanisms. All terrestrial amphibians except caeci-
Chemosensory cues for the location of prey have been lians use the tongue in capturing prey; the tongueless
inferred in various aquaüc salamanders— Notophthal- pipid frogs and aquatic salamanders have entírely differ-
mus virídescens (J. Wood and Goodwin, 1954), Gyri- ent mechanisms. Even among terrestrial anurans and sal-
nophilus porphyriticus (Culver, 1973), and Haideotriton amanders there are notably different methods of prey
waltacei (Peck, 1973). Heusser (1958) showed that Bufo capture. These differences are reflected in the diversir.
calamita could find prey solely on the basis of olfactory of the the structure of the tongue and its supportive hyo-
cues. Experiments with Bufo bóreas (Dole et al., 1981), branchial apparatus and associated musculature.
B. marínus (J. Rossi, 1983), Rana pipiens (Shinn and Many caecilians and some large, carnivorous anurans
Dole, 1978), Ambysíoma tigrinum (Lindquist and M. have long, fanglike teeth that may be curved posteriorly-
Bachmann, 1982), Plethodon cinereus (David and R. these teeth serve to hold struggling prey. In larval anc
Jaeger, 1981), and two species of Infurtís (Margolis, 1976) most neotenic salamanders, the teeth are unicuspid anc
have demonstrated that these species are capable of lo- lack the weak planes of the typically bicuspid pedicellate
caüng prey by olfactory cues alone. teeth of adult salamanders and anurans. Teeth are absen:
The role of olfaction in prey detection probably is much from the lower jaws of most anurans, and some anurans
more common among amphibians than indicated by (e.g., all bufonids) also lack teeth on the upper jaw. Many
available observations and experiments. The role of ol- frogs have a few vomerine teeth in the palate, whereas
faction in prey location, parücularly in trailing prey, is salamanders characteristically have patches of vomerine
strongly inferred by specialized chemoreceptors in some teeth that may extend posteriorly as a parasphenoid series.
amphibians—protrusible tentacles, in which the lumen The tongues of amphibians possess glands that pro-
opens to Jacobson's organ, in caecilians (Badenhorst, duce a stícky secretion that serves to adhere the prey te
1978, and references cited therein) and nasolabial grooves the surface of the tongue. Presumably in all amphibians
in plethodontid salamanders (C. Brown, 1968). The lo- except caecilians the tongue is used in prey capture, ir.
cation of termitaria by fossorial anurans such as Rhino- all groups it is used to hold the prey against the roof ce
phrynus dorsalis (Trueb and Gans, 1983) and Myoba- the mouth and to manipúlate food in the buccal cavity:
trachus gouldii (Calaby, 1956) may involve olfactory this is facilitated by secretíons of the intermaxillary glands
detection. In anurans and salamanders, food is pushed posterior*,
Experiments on Ambystoma tigrinum (Lindquist and by the contraction of the m. retractor bulbae, which de-
M.. Bachmann, 1982) and on Trituws (Margolis, 1976) presses the eye into the buccal cavity. Once food passes
show that the efficiency of detecüng, locating, and cap- the ciliated pharynx, ingestión is completed by peristahic
turing prey is greatest when both visual and olfactory action of the esophageal walls. Secretions of mucous glanos
cues are used. However, the type of prey may díctate in the buccal cavity facilítate food transport by lubricatinc
which cues are more effective. The location of pill clams the mouth and pharynx.
(Muscu/ium rosaceum) by the newt Notophthalmus vir-
idescens apparently is accomplished by olfaction alone Caecilians
(J. Wood and Goodwin, 1954). Although visual cues Terrestrial caecilians feed primarily on elongate prey, su±
predomínate in the detection of moving insects by many as earthworms, located on the surface of the ground ce
terrestrial salamanders, immobile prey such as insect pu- probably more commonly, in burrows. Prey capture r-
pae are located by olfaction in Plethodon cinereus (David volves a slow approach to the prey until contact is almos:
and R. Jaeger, 1981). Olfaction is strongly implicated in effected, at which time the prey is seized by a powerñi
the ability of Hydromantes to project its tongue at prey bite. Caecilians tend to bite the prey broadside; they mo\
in total darkness (G. Roth, 1983). the head past the prey and bite laterally. If a caeciBar
has not completely emerged from its burrow when ±>£
Auditory Detection prey is seized, it retreats into the burrow, spinning in a
Few observations are available on auditory stimuli in lo- corkscrew fashion around its body axis. This action or-
cation of prey by amphibians. Martof (1962) found that ates friction between the prey and the sides of the bir-
 Pood and Feeding
levator mandibulae externus—, I—pseudoangular 233
e»ator mandibulae anterior i—longus capitis

pseudodentary Figure 9-2. Ventrolateral view of

geniohyoideus—' cranial, hyoid, and anterior trunk
musculature of a caecilian,
genioglossus—' Dermophis mexicanas. Redrawn
-rectus cervicis from Bemis et al. (1983).

is a double-lever system with Ihe quadrale functíoning as

Ihe fulcrum. As in olher gnalhostomes, contraction of the
m. levator mandibulae (m. adductor mandibulae) results
in the lower jaw being pulled upward. The novel com-
ponenl in caecilians is Ihal contraction of the m. inter-
hyoideus posterior, which originales on Ihe fascia of Ihe
ventral and lateral body wall and inserís on Ihe venlral
surface of Ihe retroarticular process, pulís the retroartic-
ular process back and down, Ihereby causing Ihe anterior
jaw ramus to pivot upward around Ihe quadrale. A Ihird
Bfiue 9-3. Diagram of the jaw-closing mechanism of a caecilian. muscle that acts synergistically lo produce a slrong bite
Tbree distinct sets of muscles affect this unique mechanism. Dots is the m. longis capitís, a large ventral trunk muscle Ihal
xt fulera; arrows are direction of muscular contraction. originales on Ihe basapophyses of Ihe anterior vertebrae
and inserís on Ihe cranium venlral to the craniovertebral
articulation; Ihis muscle is a powerful flexor of Ihe neck
?ow, constricting and shearing the prey to approximately and cranium (Fig. 9-3).
±te width of the gape of the caecilian. Molion analyses and eleclromyography of feeding by
The tongue is not protrusible, but interspecific variation fhe caeciliid Dermophis mexicanus (Bemis el al., 1983)
«ists in the amount of free margin of the tongue and revealed Ihal during prey capture Ihe lower jaw is pressed
ríe extent of the glandular field on its dorsal surface. The againsl Ihe subslrale and íhe moulh is opened as Ihe
n. genioglossus forms the body of the tongue; it origi- cranium is raised as a resull of acüvily of Ihe m. depressor
-jates at the mandibular symphysis and from the con- mandibulae and Ihe dorsal trunk musculature. Jaw clos-
-jective tíssue overlying the m. geniohyoideus, and inserís ing is rapid and involves simultaneous conrractions of Ihe
on the surface epithelium of Ihe tongue. The muscle fi- m. levator mandibulae and m. inlerhyoideus posterior
bers in Ihe body of the tongue are dispersed vertically and presumably Ihe m. longis capitis. A single bile re-
arnong extensive blood sinuses and Ihe bases of lingual quires aboul 0.5 second. Holding onlo slruggling slippery
^ands. Contraction of these fibers (1) depresses Ihe tongue prey is facililaled by Ihe presence of two rows of long,
pad, thereby increasing pressure in Ihe blood sinuses, (2) recurved leelh in the upper jaw.
acuítales extrusión of lingual gland secreüons by com-
pressing the bases of these glands, and (3) aids in food Salamanders
Tansport (Bemis et al., 1983). Although Ihe basic srruclures are Ihe same in Ihe feeding
Adult caecilians are unique among amphibians in lack- mechanics of all salamanders, functional and develop-
Hng a m. hyoglossus and in having a complelely roofed menlal conslrainls have played an importanl role in Ihe
skull, a fixed quadrale, and a lower jaw with a long ret- modification of Ihe hyobranchial apparalus for differenl
roarticular process (Fig. 9-2). Associated with this bony kinds of feeding mechanisms. These were summarized
structure are muscles that provide a unique jaw-closing by D. Wake (1982) and are grouped into three cale-
mechanism (Bemis et al., 1983; Nussbaum, 1983). This gories.
ECOLOGY
234 Aquatic Salatnanders. In larval salamanders, neo- buccal pump mechanism in respiration and as the main
tenic adults such as proteiids, and terrestrial salamanders mechanism of tongue protrusion. Cinematographic in-
(when in water during breeding), the hyobranchial ap- vestigations coupled with morphological studies (Severt-
paratus functions to (1) support and move the gilí fila- zov, 1971, 1972; Larsen and Guthrie, 1975) provided
ments for respiratton (not so in terrestrial adults in the an interpretation of the feeding mechanisms of these sal-
water temporarily), and (2) expand and contract the buc- amanders, but electromyographic evidence is absent.
cal cavity during feeding. These movements are accom- In their analysis of the feeding mechanisms of adult
plished by the hyoid musculature in association with the Ambystoma tigrinum in the laboratory,. Larsen and Guth-
depressor mandibulae. During feeding, most salaman- rie (1975) noted that after an initial lunge the lower jaw
ders lunge toward the prey; the buccal cavity is expanded is immobilized as it is pressed against the substrate by the
and, almost simultaneously, the rather weak jaws are contraction of the m. geniohyoideus and m. rectus cer-
opened. However, in Amphiuma tridactylum, there are vicis superficialis. The cranium is elevated by the con-
two different types of suction feeding (Erdman and Cun- traction of the m. cucullaris major and the m. depressor
dall, 1984) depending on the size and activity of the prey. mandibulae. The gape is ¡ncreased further as the sala-
If the prey is small or relatively immobile, the salamander mander rocks forward, keeping its lower jaw stationary.
does not thrust its head forward; once the mouth is opened, The tongue is elevated and protruded up to 8% of the
buccal expansión induces an inward flow of water which body length beyond the margin of the lower jaw. These
sucks the prey into the mouth. The lunge or rapid strike complementan; actions seem to be accomplished by (1)
mechanism is used to capture actively moving prey. In initial propulsión of the tongue by the medial divisions oí
this strategy, mouth-opening and buccal expansión are the m. genioglossus pulling the copula of the hyoid an-
synchronous, and buccal expansión is greater than in teriorly, (2) forward projection of the hyobranchial ap-
stationary feeding. Water and prey are sucked into the paratus by the contraction of the m. subarcualis rectus I
mouth by the action of the buccal pump. The rudimen- acting on the tips of the ceratobranchials (epibranchiaií
tary tongue manipúlales the prey against the teeth on the of Larsen and Guthrie, 1975), (3) concomitant contrac-
roof of the mouth. The jaws have limited use; their small tion of the m. geniohyoideus drawing the m. rectus cer-
teeth are used to secure large prey during manipulaüon vicis superficialis and second basibranchial (Copula ü
(Matthes, 1934). anteriorly, (4) buckling of the anterior radial cartilage;
providing the form of the outgoing tongue, (5) subse-
Generalized Terrestrial Salamanders. In meta- quent shaping of the front and lateral rims of the tongue
morphosed, terrestrial salamanders having lungs (Hy- by the otoglossal cartilage and second radial cartilages
nobiidae, Dicamptodontidae, Ambystomatidae, and gen- respectively, and (6) turgidity of margins of the tongue
eralized salamandrids) the tongue is attached anteriorly, increased by fluids forced from the sublingual sinuses
is protrusible, and plays an important role in prey cap- posterolaterally into sinus pockets.
ture. The hyobranchial apparatus has a dual role as a When the prey is struck by the posterior half of th£
tongue, the lingual divisions of the m. genioglossus cor-
tract, resulting in the expulsión of a sticky secretion tria:
adheres the prey to the tongue; the m. rectus cervics
profundus then contracts causing the partial collapse ce
the anterior rim of the tongue, entrapping the prey in 2
sticky trough (Fig. 9-4). Tongue retraction is accom-
plished primarily by the m. rectus cervicis profundus are
lateral divisions of the m. rectus cervicis superficialis. Smal
prey is brought within the range of the vomerine teer.
but larger prey commonly escape from the sticky troux
during retraction and are held only by the marginal tee±-
Once the tongue has rerracted completely, the mouth is
closed by depressing the cranium sharply through ~K
contraction of the m. levator mandibulae. Immobilizarrf
of the lower jaw and opening of the mouth requirs
0.05-0.09 second, during which time the tongue pr:-
trudes; retraction of the tongue and prey requires Q.C¿
second and closure requires 0.02-0.03 second. Thus. r*
entire sequence of prey capture lasts 0.10-0.15 secorir.
Figure 9-4. Terrestrial prey capture by the salamander subsequent swallowing requires about 0.07 second.
Ambystoma tigrinum. Note the slight protrusion of the tongue with
a noticeable trough and the adpression of the mandibular
symphysis to the substrate. Drawn from a photograph in Larsen
Lungless Salamanders. Lungs are absent in sato-
and Guthrie (1975). manders of the family Plethodontidae and two genera ~
 Food and Feeding
•? amandrids, Chioglossa and Salamandrina. In these 235
z-amanders, the hyobranchial apparatus no longer func-
tons as a buccal pump to forcé air into the lungs, and
TÍ hyobranchium is modified to project the tongue from
Te mouth. Not only is the cranium elevated during feed-
rc. but the lower jaw is dropped and is not adpressed
igainst the substrate. Morphological evidence indicates
Ta: tongue projection evolved independently in sala-
-randrids and plethodontids, and within the latter group,
nghly projectile tongues evolved independently in the
-jjmidactylines and the bolitoglossines (D. Wake, 1982). Figure 9-5. Highly projectile tongue of the plethodontid
The morphology of the feeding mechanisms and their salamander Hydromantes itálicas in the capture of an insect.
Drawn from a photograph in Lombard and D. Wake (1976).
i-r.ctions have been described for salamandrids by Ózeti
«xl D. Wake (1969) and for plethodontids by Lombard
and D. Wake (1976, 1977). Electromyography of the
xjngue protrusion in one plethodontid, Bolitoglossa oc- A
záentalis, was accomplished by Thexton et al. (1977).
In those plethodontids with highly projectile tongues,
Te "projectile" consists of the tongue pad trailed by an
ecngate bundle of folded cartilages, retractor muscles,
serves, and vessels enclosed in a mucosal sheath (Fig.
?-5). In many plethodontids, the tongue pad either has
Jost the anterior attachment or has a rather elastic con- rectus cervicis profundus
•ection to the lower jaw. The hyobranchial apparatus is
romposed of elongated mobile subunits. A pair of cera-
r:c.yals that are attached posteriorly by hyoquadrate liga-
inents to the suspensoria lie on the floor of the mouth;
lt«y are not in contact with one another, ñor do they
jrtculate with any other, elements of the hyobranchium.
T~e posterior part of each ceratohyal is cylindrical and
"ooked, and the anterior part is flattened and expanded.
~~.e cartilages that move out of the mouth with the tongue
3K articulated to form a single complex unit. The prin- subarcualis rectus I
rpal element of this unit is the unpaired, median basi-
rranchial or copula. The anterior end of the basibranchial
~¿~ a projection that is either continuous with the basi-
rranchial proper or united with it by connective tissue. If Figure 9-6. Diagrammatic representation in ventrolateral view of
the tongue projection mechanism in the plethodontid salamander
Deached, the element is called the lingual cartilage. A Bolitoglossa occidentalis. A. Tongue retracted. B. Tongue
pair of radial cartilages also is attached anteriorly to the projected. Modified from Thexton et al. (1977).
-asibranchial, and two pairs of hypobranchials articúlate
•tth the posterior part of the basibranchial. The first pair
re hypobranchials are the longest elements; they articu- mer is an anterior continuation of a muscle that arises on
le with the basibranchial just posterior to its midpoint. the ischium and inserís principally into the muscular body
~-.e second pair of hypobranchials articúlate with the of the tongue. The m. subarcualis rectus I originales on
rasibranchial at its posterior end. The first and second the ventral surface of the ceratohyal and wraps around
-ypobranchials on each side approximate each other the epibranchial (sensu D. Wake) in a complex spiral,
posteriorly, and both articúlate with the ceratobranchial, forming a muscular bulb.
i tapered element of varying length. The median second Analysis of muscle action in Bolitoglossa occidentalis
basibranchial (Copula II) lies at the juncture of the m. (Thexton et al., 1977) showed that the tongue and hyoid
rectus cervicis superficialis and m. geniohyoideus; it has apparatus are projected by contraction of the m. subar-
-» connections with other elements and is lost in boli- cualis rectus I. Upon contraction of these protractors, the
z>glossine plethodontids. epibranchials are forced out of the cavity within the sub-
The tongue pad is large, and its base is supported by arcualis muscles (Fig. 9-6). Simultaneously the entire
~.e anterior end of the basibranchial. The radial and lin- muscle shortens, and the posterior end moves toward
gual cartilages extend into the pad. The principal muscles the guiar región. The forward-moving ceratobranchials
Associated with the hyobranchium are the m. rectus cer- conduct forcé via the first and second ceratobranchials
vicis profundus and the m. subarcualis rectus I. The for- to the median basibranchial and thence to the tongue
ECOLOGY
236 small prey and is accomplished rapidly (<50 millisec-
onds). Salamanders with highly projecüle tongues can
capture prey at distances equal to 44—80% of their body
length.

Anurans
The feeding mechanism of most advanced anurans in-
volves a lingual flip during which the posterodorsal sur-
face of the retracted tongue becomes the anteroventre.
surface of the fully extended tongue (Regal and Gans.
1976). In such anurans the hyobranchium provides the
mechanical base for the forceful flipping of the tongue
as such, it has a limited amount of anteroposterior move-
ment and is not projected as in salamanders. The hyo-
branchium also functions as part of the buccal pump
mechanism, as it does in generalized terrestrial salaman-
ders.
The adductor musculature is similar to that of sala-
manders, except that the m. adductor mandibulae pos-
terior is a single slip in anurans instead of two as in sal-
amanders (Salomatina, 1982). A unique feature amone
most anurans is the ability to depress the mandibular
symphysis during the lingual flip. This is possible because
of the flexibility afforded to the jaw by the presence ce
mentomeckelian cartilages and bones at the mandibular
symphysis (Fig. 9-7). Contractíon of the m. submentafis.
a median muscle extending transversely just posterior ~
the symphysis, rotates the anterior parts of the dentarles
downward and brings them closer together, thereby áe-
pressing the anterior margin of the lower jaw (Gans and
Gorniak, 1982a).
Cinematographic and electromyographic studies on the
toad Bufo marinus (Gans and Gorniak, 1982b) show r*
sequenüal steps in what is assumed to be the generalizad
feeding mechanism of most anurans. During the tongue-
flipping movement, the tongue is supported by the —
genioglossus medialis, which stiffens the tongue wher
contracted. Simultaneous contraction of the m. genio
glossus basalis provides a wedge under the anterior rr
Figure 9-7. Lingual flipping feeding mechanism in the toad Bufo of the rodlike m. genioglossus medialis. In addition tr
marinus. A. Initiation of the lingual flip. B. Fully extended tongue depressing the mandibular symphysis, the m. submer-
contacts prey. C. Partially retracted tongue with prey. Note
depressed anterior part of jaw. Adapted from Gans and Gorniak, talis acts on the wedge of the m. genioglossus basalis r:
1982a, Science 216:1335. Copyright 1982 by the AAAS. raise and rotate the rod of the m. genioglossus mediáis
over the symphysis. The üp of this lingual rod carnes
along the pad and soft tissues of the tongue. Contractior
pad. The retractors (m. rectus cervicis profundus and m. of the long, parallel fibers of the m. hyoglossus retraos
rectus abdominis profundus) are lax and lie in loops when the medial sulcus of the tongue pad and holds the prey
the tongue is in the mouth. When the tongue is projected, by a cuplike effect, which is enhanced by the sticky se-
the retractor muscles become taut; as their tensión be- cretion of the glands in the lingual pad. The extensibility
comes greater than that of the protractors, the tongue is of the buccal membranes allows the pad to be retracted
retracted into the mouth. first; the pad reaches the posterior part of the buccal
When the stícky tongue pad is projected and contacts cavity before the still-rigid, backward-rotaüng m. geniog-
a prey item, adhesión permits retracüon of the prey into lossus medialis reaches the level of the symphysis. During
the mouth. As the mouth closes, the tongue presses the this process, protraction of the hyoid facilítales the ex-
prey against the teeth in the roof of the mouth and per- tensión of the m. hyoglossus; the m. sternohyoideus re-
mits it to be manipulated and swallowed. This feeding tracts and stabilizes the hyoid when the tongue starts to
mechanism is most effective for the capture of relatively rerract; it does not function in tongue protrusion.
 Food and Feeding

1, Ifhere is considerable diversity in tongue structure among

irans (Magimel-Pelonnier, 1924; Horton, 1982b),
•xnpally involving modificatíons of the m. genioglossus.
i" tr.e archaic families, Leiopelmatídae and Discoglossi-
the flattening of the buccal floor by the m. interhyoideus
and m. intermandibularis posterior.
Essentially, these aquatic frogs suck in food and water;
the water is expelled before the mouth is closed com-
237

se. there is little free margin to the tongue. In Bomb'ma pletely. This is an effecüve mechanism for feeding on
±<s rengue can be protruded slightly, as in Ambystoma, zooplankton. Pipa and Xenopus sometimes take larger
rut presumably it cannot be flipped as in most other prey, using their long fingers to push the food into the
a-'jrans (Regal and Gans, 1976). The m. genioglossus mouth.
s rather poorly developed in some myobatrachids, and
r the aquatic Rheobatrachus the tongue is firmly at- Fossorial Anurans. Many kinds of fossorial anurans
ached to the floor of the mouth (Horton, 1982b). Some are known, or presumed, to feed underground; most of
rr ríe carnivorous frogs (e.g., Ceratophrys and Hemi- these frogs feed on ants, termites, and worms. Obviously,
yractus) that feed on large prey have exceedingly strong tongue-flipping is not a useful mechanism underground
rar.dibular symphyses with dorsally directed odontoids unless the frog is in an open burrow. Rhinophrynus dor-
ta: hold prey. Most likely, these anurans do not depress salis, a fossorial anuran that feeds on ants and termites,
tcír mandibular symphyses during feeding. Some me- not only differs structurally from other frogs but has a
arphrine pelobaüds, myobatrachids, and microhylids have unique method of tongue protrusion (Trueb and Gans,
¿srously modified tongues, but no functional studies have 1983). The contracüon of one intrinsic tongue muscle,
rccn perfomned. However, feeding mechanisms have been m. hyoglossus, results in reshaping the tongue from a
scudied in two groups of anurans that differ significantly fíat, triangular structure to a rodlike tube by stiffening the
rom the tongue-flipping mechanism. tongue and exerting hydrostatic pressure on the fluids in
the lingual sinus. Actual protrusion of the tongue is ac-
Pipids. The completely aquatic pipids are unique among complished by a forward shift of the hyoid píate and
s-.urans in lacking tongues. The hyobranchial apparatus cornua, from which the m. hyoglossus originales. This
jr.d associated musculature are quite different from that forward movement is accomplished by contraction of the
r. anurans which have tongues (Chaine, 1901; Trewa- m. geniohyoideus and apparently is facilitated by con-
•¿as. 1933). The aquatic feeding mode of pipids (Hy- traction of the m. mandibulomentalis, which elevates the
".enochirus, Pipa, and Xenopus) is accomplished by buccal floor. Retraction of the tongue is accomplished by
ransportarion of the food into the mouth with water cur- contraction of the m. sternohyoideus, which retracts the
rents produced by hyobranchial pumping movements hyoid, and the subsequent relaxation of the m. hyoglos-
Sokol, 1969); essentially these are the same movements sus.
riaracteristic of anuran larvae. Compression of the buc- Presumably Rhinophrynus positions itself with its highly
ropharyngeal cavity results from the protraction of the glandular, elongate snout just penetrating the wall of a
"ryobranchial apparatus by the m. geniohyoideus and by termitarium or termite tunnel (Fig. 9-8). As termites are

Figure 9-8. Burrowing toad,

Rhinophrynus dorsalis, showing the
calloused tip of the snout and the
opening of the buccal groove through
which the tongue protrudes. Photo
by L. Trueb.
ECOLOGY
238 detected, the tongue is protruded through a groovelike
vault in the buccal ceiling. Prey are enfolded by the cup-
shaped, villous lingual tip and withdrawn into the mouth.
The opposite is true in Rhinophrynus dorsalis, in which
the tongue and its protrusion mechanism are highly spe-
cialized for the ingestión of small prey.
With some notable exceptions, amphibians that have
generalized feeding mechanisms are active foragers with
I
EVOLUTION OF PREY-CAPTURING highly diverse diets, whereas those that have specialized
MECHANISMS AND STRATEGIES feeding mechanisms tend to use a sit-and-wait strategy.
The feeding mechanisms of living amphibians have evolved The latter include many kinds of semiaquatíc, terrestriaL
in response to natural selection and phylogenetic con- and arboreal anurans and hemidactyline and bolitoglos-
straints, and are limited somewhat by the involvement of sine salamanders. Most of these amphibians are cryptic
the hyobranchial apparatus in both feeding and ventila- and nocturnal. Because of their ability to extend the tongue
tion. Moreover, striking differences exist in the metabo- for modérate to great distances, these amphibians can
lism and energy budgets among amphibians. The dual afford to sit and wait untíl suitable prey come within strik-
function of the hyobranchial apparatus leads to inter- ing distance of the tongue, or sufficiently cióse that the
relationships that affect the foraging strategies of am- amphibian needs to move only a short distance before
phibians, but these aspects of amphibian biology are poorly capturing its prey and retuming to its feeding site. Selec-
understood. tion of a suitable feeding site is a criücal aspect of success
as a sit-and-wait predator. Observations on Rana pipiens
Morphological Constraints by Dole (1965) and on R. septentrional® by Kramek
on Foraging Tactics (1976) showed that these frogs would move farther from
Various evolutionary lineages of amphibians have evolved the feeding site for a large prey Ítem than they would for
specialized feeding mechanisms that are effecüve in ob- a small one. Moreover, if feeding success was low, the
taining prey of certain sizes and/or shapes under given frogs moved to a different site. Capture success in R.
environmental conditions. How do these funcüonal spe- septentrionalis was higher (84%) for slow-moving aphids
cializaüons correspond with (1) the kind of prey that are and chrysomelids than for aerial insects (16% for dra-
eaten and (2) the tactícs used to obtain the prey? gonflies and damselflies).
The size of the gape is an importan! factor; obviously, Among the notable exceptions are various groups or
smaller amphibians are limited to smaller prey than spe- anurans that are ant specialists (Toft, 1980a). These in-
cies that are much larger, but within size classes, some clude many dendrobatids and bufonids, all of which have
species have much smaller gapes than others. This is noxious or toxic skin secretions (see Chapter 10). These
especially evident in comparing ant-eating specialists, such active foragers with their effectíve anüpredator mecha-
as many microhylid and dendrobatid frogs, with terres- nism are "released" from the constraints of the cryptic
trial leptodactylids and ranids that feed on other kinds of innoxious anurans that use the sit-and-wait strategy to
prey. The former have relaüvely small gapes and are obtain food. However, other ant specialists, notably some
limited to small prey, of which ants are the most abun- microhylids, are cryptic and seem to search for ant traik
dant. The larger gapes of other anurans allow ingestión presumably these trails are located by olfactíon. Once an
of larger prey; these frogs have a more diversified diet ant trail is found, these anurans tend to sit and wait and
including large as well as small prey. pick up ants as they pass by. A similar strategy presum-
The generalized feeding mechanisms of some ter- ably is used by fossorial ant and termite specialists such
restrial salamanders (hynobiids, ambystomatids, most as Rhinophrynus and Hemisus. Most large predatory frogs
salamandrids, and desmognathine and plethodontine also have adopted a sit-and-wait strategy. At least in Cer-
plethodontíds) and archaic frogs (leiopelmatids and dis- atophrys this behavior may be enhanced by pedal luring.
coglossids) involve only slight protrusion of the tongue, the habit of vibrating and undulatíng the fourth and fifth
subsequent manipulaüon of the prey by the tongue against toes of the elevated hindfoot, thus attracting smaller am-
the vomerine teeth, and use of the jaws. The size of the phibians toward the Ceratophrys (Murphy, 1976).
prey seems to be limited solely by the gape. In caecilians,
gape is a major factor when feeding on the surface, but Physiological Constraints
posiüoning and shearing the prey also are importan! when on Foraging Tactics
feeding underground. Most anurans that capture prey by Two aspects of physiology are important in feeding—
a lingual flip and salamanders that have a projectile tongue energy metabolism and energy budgets. In some am-
have a further constraint—the load-bearing capacity of phibians, such as Bu/o, lactate producüon is low (see
the extended tongue. Thus, amphibians that extend the Chapter 8), so these animáis are capable of long penóos
tongue may be limited in the size of the prey that they of sustained acüvity. Other amphibians, such as Hy/a anc
can hold and retract. Carnivorous frogs that ingest large Rana, produce large amounts of lactic acid and are ca-
prey lunge at their prey while extending the tongue and pable of bursts of activity over short periods of time. Aí
use their jaws to secure the prey; thus, they do not rely first pointed out by Toft (1980a), these metabolic atrn-
solely on the tongue as the prey-capturing mechanism. butes may be correlated with foraging strategies. Thuí
 Food and Feeding
active foragers are species that are capable of sustained, varying in abundance, either temporally or spatially (Pyke 239
low levéis of activity, whereas sit-and-wait strategists are et al., 1977; Krebs, 1978). Optimal diet includes the kinds
capable of bursts of activity. The few species that have of prey which, if eaten whenever encountered, will max-
been studied metabolically conform to this dichotomy, imize the intake of caloric valué per unit time. Optimal
but a wide range of taxa need to be examined before prey choice depends on the predator's ability to distin-
any generalizations can be made. guish among prey of varying profitability and to choose
Little is known about energy budgets of amphibians. the more profitable kinds. Ideally, the predator needs
G. Smith (1976) assumed an assimilation efficiency of information about six more or less constant valúes in
74% for Bu/o terrestñs with approximately half of the order to evalúate the caloric profitability of a kind of prey
energy going into metabolic costs. In the salamander (R. Jaeger and Barnard, 1981): (1) gross calones per
Plethodon cinereus, digestive efficiency does not change prey; (2) predator's assimilation efficiency; (3) rate of
with size or sex, but caloñe intake increases with size digestión of prey; (4) calones expended in pursuit of the
iCrump, 1979). Also, digestive assimilation is negatively prey once encountered; (5) probability of capturing the
correlated with temperature in this species and in P. prey once pursued; and (6) calones expended in han-
shenandoah (Bobka etal., 1981). However, assimilation dling the prey once captured. The most profitable kind
efficiency also varíes with the kind of food. Assimilation of prey gives máximum valúes for 1, 2, 3, and 5, and
efficiency by Scaphiopus couchü is 90% when fed on mínimum valúes for 4 and 6. When the most profitable
Tenebrío larvae but only 69% when fed on Tenebrio kind of prey is abundant and easy to capture, the energy
beetles, which contain proportionately more indigestible expended per search time is low, so theoretically the
chitin (Dimmitt and Ruibal, 1980). predator can maximize net energy gain by specializing
Rates of food consumption are highly variable. The on that kind of prey. As the abundance of that prey
scmiaquatic hylid frog Acris crepitara is active for about decreases and energy per search time increases, the
7 months and feeds by night and day (B. Johnson and predator can maximize net energy gain by expanding its
Christiansen, 1976). These frogs contain an average of diet to include the next most profitable kind of prey.
6.74 prey Ítems in the stomach, and the rate of food When all kinds of prey are scarce, the predator must be
passage through the digestive system is about 8 hours. indiscriminate in its choice of diet in order to maintain a
Thus, it was calculated that each frog consumes about positive energy budget.
20 prey Ítems per day. Food consumption was greater in The only empirical tests of these ideas using an am-
larger individuáis, females, breeding individuáis, and frogs phibian are included in R. Jaeger and Barnard's (1981)
with small fat bodies. It seems that this small frog must study on Plethodon cinereus. They found that the sala-
feed nearly continuously throughout its activity season in manders had an indiscriminate diet at low prey densities
order to maintain a positive energy budget. This is in and specialized on larger prey at high densities, but at
striking contrast to some desert anurans that are active such times the salamanders did not exclude small prey.
for only short periods of time during the year. On the Also, salamanders switched from pursuit to sit-and-wait
basis of diet, stomach capacity, and energy budgets, tactics with increasing prey density. R. Jaeger and Bar-
Dimmitt and Ruibal (1980) concluded that Scaphiopus nard (1981) concluded that the salamanders compromise
couchii (which may consume termites equal to 55% of between maximizing net energy while foraging and mini-
its body weight at one feeding) is capable of consuming mizing the time for passage of prey through the digestive
enough food at a single feeding to provide it with energy tract; small prey (in this case, flies) take longer to digest
reserves for 1 year. Other desert-dwelling anurans are than larger flies because of their proportionately larger
not so efficient; S. mu/tip/icatus requires 7 feedings, and exoskeletons. Experiments on feeding of Bu/o marínus
various species of Bu/o require 11-22 feedings in order by Heatwole and Heatwole (1968) revealed that hungry
to accumulate sufficient fat reserves and other necessities toads selected larger prey, but as the toads became sa-
(e.g., trace elements and electrolytes) for 1 year. Because tiated they selected smaller prey.
of fluctuating availability of prey or environmental limi- Therefore, digestive time, as well as assimilation effi-
tations (e.g., dry weather), amphibians may not be able ciency, is important in regulating the net energy gain from
to feed effectívely throughout their season of activity. Thus, a given amount of food in a given amount of time. The
R. Jaeger (1980) found that some individuáis of Pleth- energy gained from any feeding sequence determines the
odon cinereus were existing on negative energy budgets amount of energy available for a subsequent (although
during hot, dry weather. not necessarily sequential) feeding without drawing on
fat reserves. In this context, a sit-and-wait strategist ca-
Interrelationships of Foraging pable of ingesting large prey uses very little energy in

t
_ Strategies and Constraints obtaining food and obtains large quantities of energy from
\ animal must maintain a positive energy budget in a given prey. Therefore, amphibians such as Ceratophrys
>rder to grow, reproduce, and survive periods of inactiv- and Pyxicephalus need to eat inñvquently. Peder (1983)
ty. Optimal foraging behavior of predators vanes when suggested that low metabolic rates, relatively large energy
hey have a choice of prey differing in quality and/or reserves, and thus profound resistance to starvation en-
ECOLOGY
240 able plethodontíd salamanders to survive indefinite pe- The different feeding mechanisms that evolved in di-
riods between feedings. On the contrary, amphibians that verse lineages of amphibians, whether these be the highly
actívely search for prey and consume small prey Ítems projectile tongues of bolitoglossine plethodontid sala-
(e.g., Dendrobates) must maintain a contínuous feeding manders or the paedomorphic conditions of pipid frogs,
schedule in order to maximize fitness. Those amphibians simultaneously increase the effectíveness of capturing
that have evolved highly specialized feeding mechanisms particular prey and impose rnorphological constraints. The
specialize on small prey, of which ants are the most abun- more complex a rnorphological mechanism, the more
dant; many feeding specialists have diets composed en- rigid its associated physiological attributes and behavioral
tirely of ants. In at least three species of dendrobatids, traits. The foraging strategies of species may be affected
predation on ants is correlated with high aerobic acüvity, by proximal temporal variation in both prey abundance
low anaerobic capacity, and high resting metabolism, as and the physical environment. Ultímately, the feeding
contrasted with the sit-and-wait strategist, Eleutherodac- tactics employed by any organism are constrained by the
tylus coqui (Taigen and Pough, 1983). morphological mechanisms available to the species.
 CHAPTER 1O
:t appears that almost anything wíll eat an
&nphibian!
Kennet/7 fi. Porter (197Z)
Eiieuiies aod
Defense

A Lmphibians, like all other animáis, are subject to a

great variety of predators, parasites, and diseases. Little
salamanders; causative agents have not been identified.
Also, causes are unknown for many kinds of benign tu-
Information is available on the debilitating effects of path- mors that arise mainly in soft tissues.
ogens or parasites on individual amphibians or on pop-
ulaüons in nature. On the other hand, amphibians are Bacterial Infections
known to be importan! components of the diets of many Diverse bacteria infecí amphibians. At least among labo-
tónds of predators. This must have a profound regulatory ratory specimens, the most virulent bacterial infection is
effect on populations of these amphibian prey species. caused by Pseudomonos (Pseudomonaceae). These
This chapter summarizes briefly the exisüng knowledge bacteria commonly are associated with Bacillus, Proteus,
of amphibian diseases, parasites, and predators and dis- haementerococci, and various staphylococci. All of these
cusses more thoroughly the defensive mechanisms of infect amphibians primarily by way of polluted water and
amphibians. secondarily by way of infected food. Septicemia or "red-
leg" is caused by Pseudomonas; this fatal inflammation
is not restricted to the skin but also affects the lungs,
DISEASES spleen, intestíne, and kidneys. There is some evidence
Amphibians are subject to many diseases—viral, bacte- that Pseudomonas and other aerobic bacteria are facul-
rial, and fungal, including forms of tuberculosis and cán- tatively psychrophilic and are especially detrimental to
cer. Amphibian diseases were reviewed by Reichenbach- hibernating amphibians (A. H. Carr et al., 1976).
Klinke and Elkan (1965), Elkan (1976), L. Marcus (1981), Amphibians living in association with human habita-
and G. Hoff et al. (1984). tions in the tropics may become infected with Salmonella.
As many as seven species of Sa/mone//a were found in
Viral Infections the toad Bu/o marinus in Panamá (Kourany et al., 1970).
Since Lucké's (1934) discovery of a renal adenocarci- Mycobacteria cause lesions in amphibians; the lesions
noma in Rana pipiens, numerous workers have investi- are analogous to human tuberculosis. Those mycobac-
gated the viral nature of amphibian tumors (see Elkan, teria that infect amphibians are ubiquitous saprophytes
1976, for review). Herpes-like and other viruses have commonly present on the moist skin. Infections seem to
been associated with some cases of carcinoma. A lym- occur only in debilitated or injured animáis. External le-
phosarcoma was described in Xenopus /aeuis and in some sions may develop at the sites of wounds; in the case of
241
ECOLOGY
242 lesions on the extremities, the infecüon spreads via the dence from píate tectonics, Metcalf s ideas now seem far
lymphatic channels to the visceral organs, especially the more plausible; a modern review of the distributíon of
kidneys. Infections of mycobacteria resulüng from injuries opalinids and their hosts might provide support for Met-
to the mouth may develop into tuberculosis of the bron- calf s early theory.
chi and lungs. Entamoeba occur in the digesüve tracts of amphibians
and occasionally encyst in the liver.
Fungal Infections TVypanosoma are common blood parasites of amphib-
Many kinds of fungi apparently enter amphibians' bodies ians, and hemogregarine parasites are known to occur in
via minor abrasions or through the nostrils. Once estab- the bloodstream of amphibians. The former may be
lished in the body, the fungi spread and eventually trans- transmitted by blood-sucking leeches, and the latter are
form vital parenchymatous organs into fungal granulo- transmitted by blood-sucking insects. Malaria (P/osmo-
mata, resulüng in death. The principal fungi infecüng adult dium) has not been reported in amphibians, although the
amphibians are strains of Basidiobolus, Cladosporium, vectors, Anopheles mosquitoes, have been observed bit-
Hormisdum, and Phialophora (Elkan, 1976). ing anurans.
Various fungi are saprophyüc on dead amphibian eggs,
but two species are parasitíc on nonaquatic eggs of neo- Helminths
tropical anurans (Villa, 1979). Tadpoles also are subject Intestinal worms of the phyla Platyhelminthes, Nemata,
to lethal infections of fungi; Bragg (1962) noted the para- Nematomorpha, and Acanthocephala are common para-
sitic fungus Saprolegnia infecüng three species of tad- sites of amphibians. Yamaguti (1959-63,1971) and Tuff
poles in temporary ponds. The yeast Candida humicola and Huffman (1977) provided compilations of hosts and
seems to be parasiüc in young tadpoles of the green frog, distributions of helminth parasites in amphibians. Pru-
Rana clamitans, and a mutualistic symbiont of large tad- dhoe and Bray (1982) provided a review of platyhel-
poles (Steinwascher, 1979). minth parasites of amphibians, and D. Brooks (1984)
summarized the biology, hosts, and distributions of platy-
helminth parasites of amphibians.
PARASITES One genus of monogenetic trematode, Polystoma, is
Many kinds of external and internal parasites are asso- highly host-specific in anurans worldwide; usually it in-
ciated with adult and larval amphibians, and some insect habits the urinary bladder. Many kinds of digenetic tre-
larvae parasitize amphibian eggs. No review of amphib- matodes parasitize amphibians. Intermedíate larval forms
ian parasites exists, but Elkan (1976) summarized some (cercana or metacercaria) commonly encyst in the skin
of the literature concerning endoparasites of adult am- or internal organs, especially in aquaüc amphibians, in-
phibians. The following account is organized taxonomi- cluding larvae. Common intestinal trematodes include
cally by parasites. Optethoglyphe, Glypthelmins, and Do/ichosaccus in anu-
rans and Batrachocoelium in salamanders. Species of
Protozoa Brachycoelium were reported in 25 species of North
According to Elkan (1976), amphibians invariably have American salamanders (Dyer and Brandon, 1973). The
some degree of infestaüon by protozoans, which may pulmonary trematode Haematoloechus has a worldwide
cause debilitatíon or death if they penétrate vital organs distribution in anurans. Trematodes either share the host's
or become too abundan!. However, protozoans com- food or live on desquamated epithelium, mucus, blood,
monly live symbioücally with amphibian hosts. Never- or body fluids. Apparently the hosts have neither hu-
theless, massive infecüons by sporozoans can be cata- moral ñor cellular defenses against these parasites. Once
strophic to amphibian populations, as in the case of the the parasite has invaded the body of the host, walling off
microsporidian Pleistophora, normally a parasite of in- the parasite seems to be the only protection. Encysted
sects and fishes, which was responsible for a lethal epi- cercaría remain viable and resume their life cycles when
demic among populaüons of the toad Bufo bufo in south- the amphibian has been eaten by a predator. The diver-
ern England (Canning et al., 1964). Infestaüons of the sity of digenetic trematodes parasitizing amphibians is
sporozoan Charchesium cause clogging of the gills and suggestive of coevolution of hosts and parasites, as sug-
spiracle in tadpoles, resulüng in developmental retarda- gested for plagiorchoid trematodes and anurans by D.
tion and death. Brooks (1977).
Several genera of flagellate protozoans occur in the Cestodes are uncommon but persisten! gastrointestinal
intestinal tracts of amphibians. Most of these are com- parasites of amphibians. Nematotaenia is common among
mensals, and by far the most abundan! and widespread Eurasian anurans, and larvae of several species of Di-
are species of the multíflagellate Opalina. Metcalf s (1923a) phyllobothrium infecí anurans and salamanders in North
work on the group resulted in his (1923b) suggesting that America, where Batrachotaenia and Proteocephalus also
these protozoans provided evidence for the "southern parasitize salamanders. Chlamydocephalus is a common
dispersal" of some groups of anurans, a hypothesis soundly intestinal cestode in Xenopus laevis. Tyler (1976) noted
criücized by Noble (1925b). However, in the light of evi- that in Australia anurans are second intermediate hosts
 Enemies and Defense
•or spargana larvae of tapeworms of the genus Spiro- lymph sacs or the body cavity, where they feed on blood 243
inzra. The life cycle of this cestode involves (1) eggs in the liver and heart.
•xsed from carnivorous mammals, (2) aquatic devel-
jcncnt of a coracidium larva that is eaten by an aquaüc Arthropods
=*_stacean, (3) a procercoid stage in the haemocoel of Several groups of arachnids parasitize terrestrial amphib-
•toe ;rustacean, (4) ingestión of the crustacean by a frog, ians. Ereynetid mites of the subfamily Lawrencarinae oc-
m *-hich the parasite develops into a sparganum stage in cur only in the nasal passages of anurans (Fain, 1962).
mscle or connective tissue, and (5) ingestión of the frog Chigger mites (Trobiculidae) and ticks (Ixodidae), espe-
». a mammal, in which the life cycle is completed as a cially Amb/yomma, are common blood-sucking ectopar-
apeworm. asites of terrestrial amphibians, especially those in dry
Numerous nematodes probably are the most common forests. Habitat selection by amphibians may be associ-
neminth parasites of amphibians. Some, such as the lar- ated with the degree of infestation by chiggers. Or, dif-
iaé of Filaría, are microscopic, but most, such as the ferential toxic or mucous secretions of the skin may have
lingworm (Rhabdios), are macroscopic. Nematodes are an effect on chiggers. For example, among three syntopic
icund in the gastrointestinal tract, lungs, blood vessels, species of salamanders, two species (Plethodon dorsalis
H-jd lymphaüc channels; the worms encyst in the intes- and P. g/uíinosus) are rarely infested by chiggers of the
iral wall, skeletal muscle, or any parenchymatous organ. genus Hannemania, whereas P. ouachitae is infested
riost specificity may be much lower in nematodes than heavily (Duncan and Highton, 1979). Toads (Bu/o) com-
ÍE digenetic trematodes and cestodes. For example, a monly have many ticks. As noted for B. marinus by G.
zBmocercid nematode, Cosmocerca brasi/iensis, is known Zug and P. Zug (1979), Amb/yomma are attached mostly
o parasitize 15 species of South American anurans (Dyer on the head, particularly on or adjacent to the parotoid
srd Altig, 1976), and another species, Cosmocercoides glands. When the ticks fall off, they leave small lesions.
Ojicei, is known from 14 salamander hosts in North Parasitic copepods of the genus Argu/us, or fish lice,
America (Dyer and Branden, 1973). are common ectoparasites on fishes. They have been
Adult acanthocephalans attach themselves to the mu- reported on two North American aquatic amphibians—
CDUS lining of the stomach or intestine. The most com- the salamander Pseudobranchus síriatus and tadpoles of
•»n adult form in amphibians is Acanthocephalus ranae. Rana heckscherí (C. Goin and Ogren, 1956).
7ne first intermedíate hosts of acanthocephalans are small The peculiar vermiform arthropods of the order Pen-
oustaceans or insects; adult or larval amphibians become tastomida (tongue worms) occur in the intestinal tract of
riected upon ingesting these intermedíate hosts. How- amphibians.
aver, some acanthocephalans have a second intermedi- The only group of insects that parasitize amphibians is
ae stage. This encysted stage of Porrochis is known in Díptera. Several groups of flies deposit their eggs on the
some Australian anurans; the adult stage is known only bodies of anurans or on terrestrial eggs, and the larvae
n birds. parasitize the frogs or the embryos. Tachinid flies lay their
eggs on the bodies of anurans. Upon hatching, the larvae
Annelids of Batrachomyia, endemic to Australia, burrow under the
Blood-sucking leeches (Hirundinoidea) are common ex- skin of the back (Tyler, 1976). Larvae of Luci/ia move
smal parasites on amphibians that live in or enter water to the anuran's head and enter the body by way of the
n breed; these leeches also attach themselves to aquatic eyes or nostrils and devour the host. Of 14 cases of Lu-
iarvae. Terrestrial leeches parasitize terrestrial anurans in ci/ia infections in four species of European anurans re-
±e wet tropics from southeastern Asia to northern Aus- ported by Meisterhans and Heusser (1970), only one frog
tralia. In most cases parasiüsm is temporary and probably survived.
does not interfere drastícally with the health or activity of Larvae of some flies of the families Calliphoridae, Chi-
the host. However, in some cases many leeches attached ronomidae, Drosophilidae, Ephydridae, Phoridae, and
so an individual can be debilitating, as noted by Waite Psychodidae parasitize the eggs of amphibians (Villa, 1980;
1925) for the frog Limnodynostes dumeri/i during the Villa and Townsend, 1983; Yorke, 1983). In all cases the
breeding season in South Australia, and by Gilí (1978) eggs are nonaquatic, although larvae of the ephydrid
íor the newt Notophthalmus virídescens in North Amer- Gasírops feed on embryos of Leptodacíy/us pentadac-
ica. ty/us and Physa/aemus in foam nests floaüng on the water.
Some other leeches gain access to the subcutaneous These parasitic flies lay their eggs immediately below the
lymph sacs and remain as endoparasites. Leeches of the surface of the amphibian egg mass. Timing of hatching
genus Batruchobdella are common ectoparasites of aquatic of the fly larvae must coincide with early stages of em-
anurans, but occasionally the leeches do enter the lymph bryonic development of the host, for advanced anuran
sacs of Rana catesbeiana at least. Leeches of the genus embryos are capable of muscular movements thwarting
Philaemon (Cedbdella) are unique in entering the cloaca attacks by the fly larvae. The larvae pupate in the egg
of terrestrial and arboreal frogs in New Guinea (Mann mass. These flies are known to parasitize the egg clutches
and Tyler, 1963); once inside the body they reside in of various tropical anurans, including the arboreal clutches
ECOLOGY
244 of Agalychnis, Centrolenella, Polypedates, and two spe- The arboreal eggs of phyllomedusine frogs are eaten by
cies of Hyla and the terrestrial clutches of Dendrobates nocturnal colubrid snakes of the genus Leptodeira
and Eleutherodactytus. Also, phorid larvae are known to (Duellman, 1958). These snakes manipúlate their jaws
parasitize the terrestrial eggs of one plethodonüd sala- around part of a clutch of eggs and continué to engulf
mander, Aneides aeneus. The presence of psychodid, the cohesive clutch.
chironomid, and phorid larvae in developing amphibian
egg clutches probably is peripheral to their usual life cycle,Larvae
but the life cycles of some ephydrid and drosophihd flies Larval amphibians are the prey of numerous kinds of
may be dependent upon amphibian egg clutches (Villa, fishes, turtles, wading birds, and small mammals. Even
1980). Infestations of larvae in egg clutches may be very passerine birds feed on tadpoles, as evidenced by Beis-
high at some places; 80% of the egg masses of Physa- wenger's (1981) observations of gray jays (Perisoreus
hemus cuvierí and up to 100% of those of Centrolenella canadensís) feeding on aggregations of Bufo bóreas tad-
fleischmanni were infested. poles. Some snakes feed on larvae; the South American
colubrids Liophis epinephelus and L. reginae are com-
mon predators on pond tadpoles, and the North Amer-
PREDATORS ican Thamnophis sirtalis and T. couchii commonly feed
Because amphibians are numerous, small to modérate in on tadpoles and salamander larvae.
size, and have soft skin, they are common prey for a Numerous aquatic insects prey on tadpoles. Larval
great variety of predators of all classes of vertebrales, as odonates (Anax and Poníala) are importan! predators
well as some arthropods; small anurans even fall prey to (Heyer et al., 1975; Caldwell et al., 1981), as are the
a carnivorous plant, the Venus flytrap (Dionaea masci- predaceous diving beetles, especially their larvae, of the
pula). Because adults of many species aggregate during genera Acilius andDystiscus (Young, 1967; Neill, 1968L
the breeding season and tadpoles and metamorphosing Water bugs (Belostoma) and water scorpions (Nepa and
young often are concentrated, at such times these am- Ranatra) suck the body fluids from captured tadpoles.
phibians provide sustenance for many kinds of predators their chief prey (Wager, 1965).
that aggregate for easily acquired meáis. No attempt has Perhaps some of the most significant predators on am-
been made to document the predation on amphibians phibian larvae are other amphibians. This is especialh.
by all of the numerous kinds of predators. Instead, major true in temporary ponds, although in streams larval sal-
predators, especially those that specialize on amphibi- amanders, Dicamptodon ensatas, prey on the tadpoles
ans—eggs, larvae, or adults—are emphasized in the fol- of Ascaphus (Metter, 1963). Studies by Heusser (1971)
lowing discussion. and Cooke (1974) in Europe and by Wilbur (1972), Cale:
(1973), Walters (1975), Morin (1981), and Caldwell et
Eggs al. (1981) in North America have shown that adult and
Aquatic eggs of amphibians are subject to predation pri- larval newts (Notophthalmus and Trituras) and larval
marily by fishes and aquatic invertebrates. In permanent Ambystoma are selective predators on a wide range o:
ponds and streams, amphibian eggs are susceptible to anuran larvae. Tadpoles of a few species, such as Cer-
fishes and aquatic invertebrates; in temporary ponds, atophrys comata, seem to be oblígate carnivores and
aquatic invertebrates are probably one of the most im- feed chiefly on tadpoles of other species, whereas other
portant predators. Aquatic invertebrate predators on sal- kinds of tadpoles (e.g., Leptodacfylas pentadactylus) are
amander eggs include the leech, Macrobdella decora, facultativo predators on tadpoles (Heyer et al., 1975).
feeding on the eggs of Ambystoma maculatum (Cargo, Xenopas laevís commonly feeds on tadpoles and smal
1960) and caddisfly larvae (Trichoptera: Ptilostomis sp.) frogs (Wager, 1963).
feeding on the eggs of the same species and on those of
A. tigrinum (Dalrymple, 1970). Aquatic salamanders also Adults
feed on amphibian eggs. Larval and adult newts (Noto- As noted by Porter (1972), practically anything will eat
phthalmus uiridescens) and larval A. opacum eat eggs of an amphibian, but the subterranean habits of most cae-
several species of anurans and salamanders (Walters, cilians preclude their exposure to most predators excepi
1975). fossorial snakes, such as coral snakes (Mientras).
Terrestrial eggs of plethodontid salamanders and vari- Various species of predaceous spiders feed on am-
ous groups of anurans are eaten by a variety of insects, phibians (see Formanowicz et al., 1981, for review). In
especially carabid and tenebrionid beetles. Furthermore, some cases the amphibians are caught in webs and sub-
plethodontid salamanders feed on the eggs of other sequently killed and eaten, but crab spiders, tarántulas,
plethodontids. Eggs in the terrestrial foam nests of Lep- and other hunting spiders spring on amphibian prey, grasp
todactylas latinosas are eaten commonly by a lycosid them, and kill by injection. Formanowicz et al. (1981
spider, Lycosus pampeana in Argentina (Villa et al., 1982). demonstrated a negative correlation between successfiL
The arboreal eggs of centrolenid frogs are consumed by predation by the crab spider (Olios) and body size of the
phalangids, graspid crabs, and crickets (Hayes, 1983). frog Eleatherodacfylas coqai. Freshwater crabs seem to
 Enemies and Defense
, on small frogs. In Panamá we observed a crab Bu/o. North American colubrid snakes of the genus Het- 245
ssing the foreleg of a Co/osteíhus inguina/is; many erodon and South American colubrids of the genus Xe-
es of this genus along streams in the Neotropics in- nodon specialize on Bu/o, and the latter also eats large
iacE&á by crabs are missing limbs. Larvae of horseflies frogs, such as Leptodacty/us pentadacty/us (Fig. 10-1).
Ticcnus punctifer) burrow tail first into mud at the mar- These snakes have large gapes and long, grooved teeth
pis of ponds; these larvae have hooked mandibles and on the maxillae; they are capable of piercing the tough
•TV recently metamorphosed spadefoot toads (Scaphio- skin of the inflated toads and killing them with venom.
JRS multiplicatus). The larvae pulí the toads into the mud Although most viperids specialize on warm-blooded prey,
•c -di them by feeding on their body fluids (Jackman juveniles of many species of vipers feed on amphibians;
«a.. 1983). adults of Agfcístrodon commonly feed on anurans, and
feong vertebrates, fishes, turtles, and crocodilians are the African Causus rhombeatus feeds exclusively on toads
aquatic predators on anurans, whereas various kinds (Bufo).
s-.akes, birds, and mammals are terrestrial or aquatic- In the tropics, where the diversity of anurans is highest,
^T! predators. Also, some anurans feed on other frogs. there are many species of snakes that feed on anurans,
carnivorous frogs, such as Cyc/orana ausíra/is, and some eat anurans almost exclusively. In África, col-
ftxeepha/us adspersus, í?ana catesbeiana, Rana tiger- ubrid snakes of the genus Philothamnus specialize on
•c. and species of Ceratophrys and Lepidobatrachus, Hypero/ius, and species of Lycodontomorphus feed ex-
me -Qtorious for their voracious appetites, which include clusively on Rana (Wager, 1965). Many neotropical col-
as. available smaller frogs. The carnivorous hylid frogs ubrid snakes feed primarily or exclusively on anurans. In
3e-tphractus commonly eat anurans; stomachs of 10 the Amazon Basin, nocturnal tree snakes Leptodeira an-
«ecimens of H. proboscídeus contained 15 frogs of 12 nulata and Imantodes lentiferus feed on active, arboreal
«ees (Duellman, 1978). frogs at night, and diurnal arboreal snakes Leptophis
Ljzards are not important predators on amphibians, ahuetulla and Oxybe/is argenteus ferret out the frogs by
atrcugh monitors (Varanus) are known to eat anurans day (Duellman, 1978). In the same región, snakes of the
<62cer. 1965). Many kinds of snakes feed on amphibi- genera Chironius, Liophis, and Xenodon actively forage
ms. and some species specialize on certain kinds of am- for anurans on the ground by day.
artcians. The colubrid Diadophis punctatus and various Wading birds, such as egrets, herons, and ¡bises, are
«asees of Thamnophis prey on plethodontid salaman- known to prey heavily on anurans in, and at the edges
•MES. and the semiaquatic natricines Natrix, Nerodia, and of, ponds, especially on species of Rana. Passerine birds
is prey on frogs. The aquatic colubrid Foronda are important predators on amphibians. R. Jaeger (1981a)
feeds almost exclusively on Amphiuma. Some observed which foraging passerines which scratch in leaf
stares specialize on heavy-bodied anurans, especially litter for prey are more efficient at finding prey when the

Figure 10-1. A colubrid snake,

Xenodon severus, an anuran
specialist, 1050 mm in body length,
swallowing a Leptodactylus
pentadactylus, 173 mm ¡n snout-vent
length. Santa Cecilia, Ecuador.
Photo by W. E. Duellman.
ECOLOGY
246

Figure 10-2. A phyllostomatid bat,

Trachops cirrhosus, about to capture
a hylid frog, Agalychnis callidryas.
Barro Colorado Island, Panamá.
Photo by M. D. Tuttle.

leaves are dry than when wet; plethodonüd salamanders, predators. However, amphibians have evolved variots
which are suitable prey for these birds, are more common morphological, physiological, and behavioral features.
in the leaf litter when it is wet. Some birds may have which alone or in combinaüon provide varying degrees
developed specialized search images or behaviors for of protecüon from potential predators.
preying on certain amphibians. For example, the South
American hawk Geranospiza caerulescens apparentiy uses Escape Behavior
its long legs and talons to extract anurans from their diur- Predation can be avoided by escaping from a potenta
nal retreats in the axils of leaves of arboreal bromeliads predator prior to an actual encounter; this usually »-
(Bokermann, 1978). volves the prey sensing the presence of a predator. Es-
Nocturnal mammals, especially raccoons (Procyon), cape may be affected by rapid movement, hiding, or a
skunks (Mephitis), night monkeys (Aotus), and various combinaüon thereof.
kinds of opossums, prey on amphibians. Also, two gen-
era of bats feed on anurans. Megoderma in the Oíd World Movement. Active escape depends on the locomotor
and the neotropical Trachops cirrhosus are attracted by capabilities of the organism. Terrestrial caecilians are sa-
anuran vocalizatíons (Fig. 10-2) (see Chapter 4). dom active aboveground, and unless they happen to be
on an impenetrable surface, they are capable of burrow-
Cannibalism ing into the soil quickly. Most salamanders move rathe
Feeding on conspecifics has been documented in several slowly, but some salamanders are capable of rapid prc-
larval amphibians, particularly among tadpoles of Sca- tean movements resulting in changes in the shape. po-
phiopus bombifrons and the larvae of Ambystoma ti- sition, or locaüon of the salamander. These flippinc
grinum, in both of which cannibalisüc morphs have evolved movements are accomplished by (1) propelling the boói
(see Chapter 6). The feeding on conspecific eggs and by a series of rapidly alternatíng coiling and uncoifing
juveniles by adult anurans and salamanders seems to movements, (2) propelling the body by flipping the tai
represen! only a predator taking advantage of an avail- while the salamander is running, or (3) lateral writhinc
able food source. There is no evidence that the predator resembling serpenüne locomoüon. The last type of
can distinguish conspecifics. Cannibalism by many kinds movement is especially developed in the extremely elor-
of tadpoles is the result of crowding and/or a limited food gate plethodonüds of the genus Oedipina.
supply. The saltatorial locomotion of most anurans is an ex-
cellent mechanism for escaping potential predators, espí-
cially those that depend on chemosensory cues for trai-
ANTIPREDATOR MECHANISMS ing prey, for the trail is interrupted by jumping in anurars
Generally, amphibians are viewed as rather defenseless This escape behavior may involve any one of severa
creatures that are consumed readily by a great variety of strategies depending on the anuran and its environmerr
 Enemies and Defense
(1) a single, long leap carrying the frog to shelter, as is amanders and the uniform or mottled green patterns of 347
characteristíc of many Rana, which leap from land to tree frogs that perch on leaves. Countershading, as in
water; (2) a single, long leap and subsequent immobility adult newts (Notophthalmus), also is important in con-
with the anuran relying on cryptic coloration to avoid cealment. Some tree frogs that perch on leaves (e.g.,
subsequent discovery, as is characteristic of many terres- species of Centrolenella and Agalychnis) reflect near-
rrial frogs (e.g., some species of Eleutherodactylus); (3) infrared light (Schwalm et al., 1977); infrared reflectance
a leap from one branch to another, as is characteristic of may be crytic coloration in that leaves also reflect in-
many tree frogs and is carried to an extreme in a few frared.
species that are capable of "parachuüng" or gliding (e.g., Disruptive coloration.—The visual search image of a
Agalychnis moreletü, Hyla miliaria, and various species predator can be confused by color patterns that do not
of Rhacophorus); (4) a series of long leaps that carry the conform to the outline of the prey. Many terrestrial and
frog a sufficient distance from the predator, as in the some arboreal anurans have a dark stripe along the side
Australian rocket frog, Litaría nasuta; (5) a prolonged of the head (even contínuing through the eye), thereby
series of short, unidirecüonal hops and subsequent im- disrupting the image of the head; also, dark diagonal
mobility, as in many Bufo; (6) a series of short, multídi- marks on the hindlimbs and chevron-shaped marks on
rectíonal hops, as in Acris at the margin of a pond or the dorsum of the body break up the outline of many
Colostethus on the forest floor or in a stream bed. terrestrial anurans (Fig. 10-4). A middorsal palé line is a
common disruptive color pattern in many species of
Cryptic Coloration and Structure. The colors, pat- Eleutherodactylus, Physalaemus, Bufo, and Rana. Like-
terns, and strucrural features of many amphibians are wise, irregular dorsal markings, such as pale-colored
importan! to their avoidance of visual recognitíon by proximal segments of limbs, of many terrestrial salaman-
predators, or créate opücal illusions that confuse preda- ders are thought to be disruptive. Tadpoles of Acris cre-
tors. pitans that develop in ponds have black tips to the tails,
Concealing coloration.—Many species of amphibians whereas those that develop in lakes and streams have no
nave colors and patterns that tend to match those of the distínctive caudal markings; the black-tipped tail seems
substrates on which they live (K. Morris and Lowe, 1964). to be an important deflective mechanism to divert attacks
These colors may be palé, lichenous markings on the by dragonfly larvae that occur in ponds (Caldwell, 1982).
dorsum that blend with rocks or tree trunks, as in the Confusing coloration.—Elongate organisms that rely
salamanders Hynobius lichenatus and Aneides aeneus or on speed to escape predators often have linear color
the tree frog Hyla arenicolor (Fig. 10-3). The dull browns, patterns that presumably créate an optícal ¡Ilusión when
grays, and blacks of many terrestrial amphibians that in- the animal is moving. Color patterns of this type are un-
habit the forest floor are effective concealing colors, as common in amphibians but do occur in caecilians of the
are the mottled patterns of bottom-dwelling aquatic sal- genus Rhinatrema and in a few salamanders (e.g., Eu-

Figure 10-3. Concealing coloration

in a hylid frog, Hyla arenicolor.
Sabino Canyon, Arizona. Photo by
J. S. Frost.
ECOLOGY
248

Figure 10-4. Disruptive coloration

in a leptodactylid frog,
Eleutherodactylus w-nigrum.
Chiriboga, Ecuador. Photo by W. E.
Duellman.

rycea and Pseudobranchus). A pattern of longitudinal Encounter Behavior

stripes is not common among anurans but does occur in Predators that encounter amphibians may be faced with
some species of Rana, Hy/a, Hypero/ius, and Ptychad- a variety of defense mechanisms that allow the amphib-
ena, all of which have rather slender bodies. Among anu- ian to escape, although it may suffer wounds in the process
rans, a more common, confusing coloration may be so- Faced with a potential predator, some amphibians ha\.«
called flash colors on the flanks and thighs, surfaces that rather stereotyped postures in which they (1) feign dear_
are concealed when the frog is at rest but that are visible (2) present a larger image to the predator, (3) confusé
when the frog leaps. These flash colors usually are vivid the predator by changing the characteristic shape of the
and contrast strikingly with the dorsal surfaces (Fig. 10- body, (4) present the predator with the least palatabie
5). Flash colors are visible only momentarily to a predator part of the body (áreas of concentrations of granula:
while the frog leaps; the frog then assumes a resting po- glands), (5) present aposematic coloration, or (6) phys-
sition and may be cryptically colored. Flash colors are cally attack the predator.
especially prevalent among tree frogs. The data on defensive behavior in terrestrial salaman-
Cryptíc structure.—Some structural features of anu- ders were discussed by Brodie (1977, 1983 and papéis
rans presen! a disruptive pattern and therefore are useful cited therein), whereas the data presented here on anu-
in concealment from predators. Bony extensions of the rans are from a variety of sources, including the earr.
squamosal provide anurans, such as Ceratobatrachus, work by Hinsche (1928), experiments by Marchisin and
Hemiphractus, and Bu/o fyphonius, with a disruptive J. Anderson (1978), and brief reviews by Lescure (1977
outline to the head. These and features such as dermal and Perret (1979); C. Dodd (1976) provided a cross-
flaps on the eyelids and heels, scalloped dermal folds on indexed bibliography of anuran defense mechanisms.
the limbs, and tubercles on the body all aid in conceal- Although some similarities exist between the behavioís
ment. Anurans such as Megophrys nasuta with tan colors of salamanders and anurans, the differences and uniqué
and irregular outlines to the body and Edalorhina perezi attributes of each group are sufficient so that the groups
with longitudinal dermal ridges and brown streaks on the are treated best individually.
body are camouflaged among leaves on the forest floor,
whereas Hy/a lancasteri with spinous tubercles and mot- Caecilians. The only reported defensive behavior by
tled green coloration is cryptic on moss-covered branches a caecilian is Sanderson's (1932:221) statement abouc
in cloud forest. Cryptic structure and/or coloration are Geotrypetes seraphini: "...it spat a small blob of water a:
most common among species that either are rather sed- me with considerable forcé. This it continued to do whü£
entary or tend to escape potenüal predators by a single I gathered it up." However, when caecilians are graspec
leap. they exude copious quantities of mucus, which maks
 Enemies and Defense
249

Figure 10-5. Flash colors in the

hylid frog Phyllomedusa perinesos.
Río Salado, Ecuador. The dorsum is
leaf green, and the flanks and hidden
surfaces of the thighs are purple with
large orange spots and small white
flecks. Photo by W. E. Duellman.

r.em extremely difficult to hold while they writhe stren- presumably reduces the probability of injury by a preda-
oously. Large caecilians are capable of inflicting painful tor that has yet to learn that the salamander is inedible
rites and deep lacerations with their teeth. Furthermore, (Naylor, 1978a).
E least some caecilians have toxic secretions (De Lille, Tail lashing.—Salamanders that lash their tails at a
1934; Sawaya, 1939; Moodie, 1978). predator have well-developed caudal musculature and a
concentration of enlarged granular glands on the dorsal
Salamanders. Brodie (1983) usted 29 antípredator surface of the tail. Aposematic coloration, if present, is
—.echanisms in terrestrial salamanders (Table 10-1) and confined to the dorsum. This active antipredator behavior
identífied four suites of correlated antípredator mecha- involves lashing the tail laterally and forcefully toward a
risms that act together (probably synergistícally) to pro- predator. Tail-lashing normally takes place with the pelvic
TKÍ salamanders from predators (Table 10-2; Fig. 10-6): región elevated by the extensión of the hindlimbs. Move-
Unken reflex.—The term comes from the onomato- ment of the tail attracts the predator to the área of con-
poetíc Germán ñame for Bombina, which produces a cali centration of glands; any attack on the tail, the most dis-
xiunding like "unk, unk, unk," and which exhibits the pensable part of the salamander, results in the predator
reflex named after it. This is a rigid, immobile posture encountering noxious secretions.
iith the chin and tail elevated so as to display bright Tail undulation.—This is a passive antipredator be-
ventral coloration. All salamanders exhibiting this behav- havior in which the tail is moved in a sinuous manner
ior are salamandrids with toxic skin secretions that ema- while the body is immobile; usually the tail is held ver-
nate from glands more or less evenly distributed on the tically while undulating and the body is coiled with the
dorsum. The toxicity and associated noxiousness protect head under the base of the tail. The tail is long and
salamanders with this suite of characters from being eaten slender with a concentration of granular glands on the
by most predators, but do not prevent predators from dorsal surface; most species have specializations for cau-
attacking. The bright coloration and distinctíve posture dal autotomy. Aposematic coloration, if present, is re-
displaying the ventral coloration are cues that are asso- stricted to the dorsum. This behavior directs the preda-
ciated with noxiousness by predators. The immobility tor's attention to the tail, which produces large quantities
characteristic of the Unken posture reduces the intensity of distasteful secretions and in most cases can be autot-
of predator attack, which increases the probability that a omized. The predator is attracted to the autotomized tail,
predator will reject an inedible salamander without inflict- which continúes to undulate; during this distraction, the
ing serious wounds. Salamanders exhibiting the Unken salamander has a chance to escape.
reflex have bony frontosquamosal arches and expanded Head butting.—Some heavy-bodied salamanders with
neural arches on the vertebrae; this increased ossification concentrations of granular glands in the parotoid región
 ose

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- 1 1 + + 1 + 1 1 1 1 + + 1 l i l i Glandular warts laterally

-+ 1 1 + + + 1 1 + + + + + ++++ Dorsum of tail glandular

- 1 1 1 1 1 1 1 1 + 1 + 1 1 • 1 + • Venter of tail glandular

- 1 1 ++ 1 I I 1 1 1 + 1 1 • 1 1 • Middorsum of body glandular

1 1 1 + 1 1 1 1 1 1 1 1 1 - I I - Secretion sprayed

—h 1 1 + 1 + 1 + + + + + + 1 1 + 1 Aposematíc coloration on dorsum

—h + + + 1 + + + + + + + 1 l i l i Aposematíc coloration on venter

1 1 1 1 1 1 1 1 1 1 1 1 1 .... Pseudoaposematic coloration

- + + + 1 I + 1 + . . ++ . . . . . Immobile posture

-+ 1 1 + 1 + 1 + . . I + . . .+ . Body coiled

1 1 1 + 1 1 1 1 • • I I Body flipped

—h + + 1 1 + 1 + • •+ + • • • 1 • Venter exposed, tail np

—h + + 1 1 + 1 + • • + + • • • 1 • Venter exposed, chin up

1 1 1 1 1 + 1 1 • • I I - • • 1 • Rolls onto dorsum

- 1 1 1 + + 1 1 1 • • I I - • • 1 • Body arched

Head buttíng

Tail lashed

—h 1 1 1 + 1 1 1 • • + 1 • • •+ • Tail wagged

-+ 1 1 + 1 + 1 + . . ++ . . . , . Tail undnlated

1 1 1 1 1 + 1 1 1 1 1 + 1 1 l i l i Ribs pierce skin

i 1 1 1 1 1 1 1 1 1 1 + 1 l i l i 1 Hook on quadrate

Vocalize

1
Bite

1 1 1 1 1 1 1 1 1 l i l i + 1 1 1 1 Tail autotomy

+++ + 1 +++ + 1 + + + l i l i 1 Frontosquamosal arch

+ 1 1 + 1 1 + 1 + 1 1 + + l i l i 1 Expanded neural spines

I )li nniplnilcinhlm' <*»*<** -••*«• etvjMHti
Dícumpíodon , . _ + -.. * 4
Rhyacotriton + - - - - + - I + -(
Ambystomatídae
Ambystoma
Rhyacosiredon
Plethodontidae
Aneides
Batrachoseps
Bolitoglossa
Chiropterotriton
Desmognathus
Ensatina
Eurycea
Gyrinophilus 1 _ _

Hemidactylium
Hydromantes
Lineotriton
Oedipina
Pawimolge
Phaeognathus
Ptethodon
Pseudoeurycea
Pseudotriton
_ _ _ 1 _ _
Thorius
Typh/otriíon
"Modified from Brodie (1983).
b + = present in at least one species; - = unknown in genus; • = no data.
ECOLOGY
252 Table 10-2. Defensive Behavior in Terrestrial Salamanders*
Unken Tail Tail Head
Genos reflex lashing undulation butting
Hynobius
Cynops
Echinotriton
Notophthalmus
Paramesotriton
Pleurodeles
Salamandra
Taricha
Trituras
Ty/ototriton
Dicamptodon
Rhyacotriton
Ambystoma
Rhyacosiredon
Aneides
Bolitoglossa
Chiropterotriton
Ensatina
Eurycea
Gyrinophilus
Hemidacfylium
Hydromantes
Oedipina
Plethodon
Pseudoeurycea
Pseudotriton
Thorius
Typhlotriton
*Data from Brodie (1983).

flex the head downward and swing the head toward, or mobilizing the snake by means of adhesive secretiors
lunge at, a predator. The body is held off the substrate, (Fig. 10-8). Observations by Amold (1982) of attacks by
and the head and anterior part of the body are inclined snakes on various plethodontíd Salamanders indícate tha:
toward the predator. Some species vocalize while engag- the defensive valué of their skin secretíons may be ac-
ing in this behavior. Aposemaüc coloration, if present, is hesive rather than toxic; the secretions produced by largc
dorsal and may be centered on the parotoid glands. This individuáis of various plethodontids can completely irc-
behavior presents the predator with the most distasteful mobilize a small snake by gluing coils together or gluin;
part of the salamander. the snake's mouth closed.
Other mechanisms.—Salamanders may defend Feigning death may be an effective defense mecha-
themselves actively once they are grasped by a predator. nism because many predators tend to take only livinc
This, most commonly, is by biting, and Pleurodeles, Di- prey. The salamandrid Paramesotriton chinensis feigrs
camptodon, Desmognathus, and some species of Am- death by rolling onto its back, thereby exposing its brighir»
bystoma bite strenuously. Amphiuma is notorious for its colored venter (Brodie, 1983).
capability to inflict deep laceratíons. Species in three gen-
era of salamandrids utilize their ribs in defensive behavior Anurans. Most anurans seem to rely on escape be-
(Brodie et al., 1984). The blunt-tipped ribs of Ty/ototriton havior to avoid predation, but some, especially speoss
elévate the lateral concentrations of granular glands. The that are incapable of rapid escape, have developed vaei-
ribs are rotated, elevated, and penétrate the skin in Pleu- ous defensive behaviors in response to encounter be
rodeles waltl and Echinotriton andersoni and E. chin- predators.
haiensis; in Echinotriton the ribs pierce concentrations of Death feigning is widespread in anurans. Among ry.-
granular glands. Also in Echinotriton a hook on the quad- lids, some species of Hy/a and Phyllomedusa tuck n£
rate pierces a concentration of granular glands (Fig. 10- limbs in cióse to the body and remain motíonless on tr.er
7). Two other ultímate defense mechanisms by Batra- back. Other anurans stretch their limbs out (Fig. 10-9i
choseps attenuatus were described by Arnold (1982). in some of these, such as Proceratophrys appendicüoi;
Some of these Salamanders grasped by small garter snakes and Stereocyclops parkeri, a stiff-legged motíonless pas-
(Thamnophis) escaped either by looping the tail around ture combined with cryptic coloration may be especalt
the snake's neck, thereby thwarting ingestión or by im- effective against visually oriented avian predators rvar
 Enemies and Defense
253

Figure 10-6. Types of antipredator

postures by terrestrial salamanders.
(Upper left) Ambystoma cingulatum;
the tai) is held across the head.
(Middle left) Bolitoglossa franklini;
the middle portion of the body is
elevated and the tail is undulated.
(Bottom left) Tarícha rivularts; the
chin, belly, and tail are elevated so
as to display the bright red ventral
color. (Upper right) Eurycea lucífuga;
the tail is undulated from this
position. (Middle right) Ambystoma
laterale; the tail is undulated from
this elevated position. (Bottom right)
Ambystoma lacustris; the tail is
lashed from this position. Photos by
E. D. Brodie, Jr.

Figure 10-7. Salamanders that use

their ribs in protection. (Left)
Echinotriton andersoni protrudes
sharply pointed ribs through
concentrations of granular glands on
the flanks. (Right) Ty/ototriíon
verrucosus has blunt-tipped ribs that
elévate the concentrations of
granular glands on the flanks. Both
species elévate the tails so as to
display bright ventral colors. Photos
by E. D. Brodie, Jr.

disturb leaf litter for food (Sazima, 1978). The hyperoliid A common defénsive behavior among heavy-bodied
Acanthixalus spinosus crouches with its limbs tucked anurans is the inflaüon of the lungs, thereby puffing up
against the body, closes its eyes, and protrudes its orange the body and presenting a larger image to a potential
tongue (Perret, 1962). predator. In species of Scaphiopus, Limnodynastes, Lep-
ECOLOGY
254 todactylus, and Bu/o, inflation of the lungs usually is ac-
companied by lifting the body off the substrate. Some
species of Bu/o also tilt the body laterally toward the
predator (Hanson and Vial, 1956). Many kinds of anu-
rans elévate the posterior part of the body and flex the
head downward toward the predator (Fig. 10-10). In Bu/o,
this posture presents the parotoid glands toward the
predator, but the other anurans that exhibit this posture
do not have concentrations of granular glands in the par-
otoid región.
Leptodactylids of the genera Physalaemus and P/eu-
rodema have large inguinal glands, and in some of these
the glands are elevated and brightly colored. Some spe-
cies of P/euradema and Physa/aemus assume a defensive
posture of lowering the head and elevating the pelvic
región, thereby presenting the glands to the predator (Fig.
10-11). The ocelli-like markings on the glands have been
interpreted as "eyespots" with the suggestíon that the
broad pelvic región with elevated "eyes" gives the image
of a much larger organism.
Some anurans gape when faced with a predator. Hy-
peroliids of the genus Leptope/is simply open their mouths
in an apparently threatening pose (Perret, 1966). The
hylid Hemiphractus fasciatus tilts the head up, opens the
mouth widely displaying an orange tongue, turns toward
the predator, and sometimes snaps at it (Fig. 10-12); a
pair of sharp odontoids on the lower jaw inflict deep
Figure 10-8. Defensive behavior by the salamander Batrachoseps punctures as the frog maintains a tenacious grip (Myers.
attenuatus toward garter snakes, Thamnophis. (Upper) Thwarting 1966). The leptodactylid Caudiverbera caudiuerbera in-
ingestión by wrapping the tail around the snake's neck. (Lower) A
Thamnophis immobilized by adhesive skin secretions. Photos by flates the lungs, elévales the body, opens the mouth.
S. J. Amold. emits loud vocalizations, and jumps at a potential preda-

Figme 10-9. Death feigning by

Eleutherodactylus curripés; the limbs
are outstretched, and the frog
remains motionless. Photo by J. E.
Simmons.
 Enemies and Defense
255

Figure 10-10. Elevation of the

posterior part of the body and
inclination of the head toward a
predator by Phrynomerus bifasciatus.
Photo by E. D. Brodie, Jr.

Figure 10-11. Defensive posture by

Physalaemus nattereri, elevating
inguinal glands toward a predator.
Photo by E. D. Brodie, Jr.

ur (Veloso, 1977); this behavior also is characteristic of cies of South American bufonids of the genus Me/ano-
Megophrys montana. phryniscus also exhibit this behavior (Cei, 1980). Like
The Unken reflex posture of arching the back with the Bombina, these small toads have brightly colored venters
head and posterior part of the body elevated while re- and many granular glands on the dorsum.
maining motionless and displaying the brilliantly colored Vocalizatíon may be used in defense (see Chapter 4).
venter is well known in Bombina (Fig. 10-13). Two spe- However, advertisement calis may attract predators, in
ECOLOGY
256

Figure 10-12. Mouth gaping by the

horned hylid frog, Hemíphractus
fasciatus, exposing the bright orange
tongue. Photo by C. R. Schneider;
courtesy of C. W. Myers.

Figure 10-13. Unken reflex ¡n

Bambino variegata, showing frog
resting on its belly with chin elevated
and palms and soles, which are
bright orange, upturned. Photo by
E. D. Brodie, Jr.

which case some species of anurans have modified call- alis and Scaphiopus and also have been reported ir. var-
ing behavior in response to the presence of predators; ous other anurans, includingPe/obates/uscus, Litare ar-
for example, chorusing Physalaemus pustulosas detect rea, and various species of Phyllomedusa. There s w
predatory bats visually and termínate calling within a sec- experimental evidence on the effects, if any, of th
ond after the arrival of a bat over the pond (Tuttle et al., odors on potenüal predators; possibly the odors are
1982). Some frogs produce odors that are disagreeable sociatíve cues.
(to humans); these are well known in Rana septentrion- Ultímate defense mechanisms include bitíng, which :
 Enemies and Defense
be most effective in some large-headed species with strong appeared at metamorphosis and that in at least one spe- 257
•aws, such as Pyxicephalus adspersus and species of Cer- cies, Rana sylvatica, noxiousness was correlated with the
ctophrys. Also, some African ranids of the genus Pty- development of granular glands.
:hadena have the terminal phalange of the third toe
rr.odified as a spine that protrudes through the skin; pos- Skin Toxins. The taxonomic distribution and bio-
sbly this is used in defense, because kicking by the frog chemical composition of the skin toxins of amphibians
zould result in lacerations of the predator. There have only now are being discovered, although the toxic prop-
been many reports of anurans emptying their bladders erties of some dendrobatid frogs and salamandrids have
A'hen grasped by a predator; this may be a reaction to been known for more than 100 years.
extreme stress, and there is no evidence that the bladder Caecilians.—Sawaya (1940) demonstrated toxic
*ater causes the predator to reléase its grasp. properties of a compound (siphonopsina) in the skin of
Siphonops annulatus. Experiments with the aquatic cae-
Noxiousness and Toxicity cilian TypWonectes compressicauda by Moodie (1978)
Presumably, all amphibians have two kinds of glands in revealed that the secretions were toxic to a coexisting
fie skin, namely mucous and granular glands. Mucous predatory fish, Hoplias malabaricus.
^ands are distributed throughout the integument, and Salamanders.—Most salamanders having toxic secre-
iheir secretions provide the moist coating necessary for tions are members of the family Salamandridae. The ma-
rutaneous respiraüon (see Chapter 8). Granular glands, jor toxin in Taricha and Notophthalmus is the neurotoxic
¿so referred to as serous or poison glands, may be dis- tetrodotoxin (tarichatoxin); salamandarin alkaloids caus-
ributed evenly or concentrated in certain áreas of the ing muscle convulsions are present in Salamandra. The
body; in some species the granular glands secrete sub- secretions of tarichatoxin from T. granulosa are highly
sances that are noxious or even toxic, thereby rendering toxic; an adult T. granulosa has sufficient toxin to kill
r>.e amphibian unpalatable to some predators. Some of approximately 25,000 white mice (Brodie et al., 1974).
riese secretions also might be effective against bacterial The two species of the plethododontid genus Pseudotrí-
and fungal infecüons (Bachmeyer et al., 1967), because ton are the only nonsalamandrids known to produce tox-
at least some of them contain antimicrobial actívity ins (Branden and Huheey, 1981). The proteinaceous toxin
Pruesser et al., 1975). Pharmacologically active sub- of Pseudotriton has a high molecular weight, unlike the
sances in the skin of amphibians range from simple amines weights of other salamander toxins, except the heavy
and derivatives) such as norepinephrine and histamine proteinaceous toxin of Trituras cristatus (Jaussi and Kunz,
:o biologically active peptides, piperidine, and steroidal 1978), although Branden and Huheey (1981) noted heavy
alkaloids, bufodienolides, and tetrodotoxin (see reviews toxins in other North American salamandrids. The effect
by Michl and Kaiser, 1963; Erspamer, 1971; Daly and of pseudotritontoxin on mice is primarily severe hypoth-
Witkop, 1971; Daly et al., 1978; Daly, 1982). ermia.
Evidence for the noxious and toxic propertíes of se- Anurans.—A wide variety of toxins of relatively low
cretions from the granular glands has been derived from molecular weights have been identified in numerous anu-
observations on predator-prey interactions (e.g., Brodie rans, although a toxin with a high molecular weight has
etal., 1979; DiGiovanni and Brodie, 1981) and from the been found in Bombina varíegata (Bachmeyer et al.,
isolation of compounds from the secretions and the de- 1967). Substances such as bradykinin, caerulin, lepto-
-.ermination of the toxicity of compounds by the injection dactylin, physalaemin, phyllokinin, sauvagine, and sero-
of compounds into laboratory mice (e.g., Daly et al., 1978; tonin have been isolated from the skins of a wide variety
Branden and Huheey, 1981). Human taste is a sensitive of anurans (Erspamer, 1971; Erspamer and Melchiorri,
indicator of the presence of pharmacologically active sub- 1980; Nakajima, 1981). These compounds may serve a
stances in amphibian skin (Myers and Daly, 1976; Myers defensive function when present in large quantities. Some
et al., 1978). Noxious secretions of at least some species of these have vasoconstrictive or hypotensive actions.
apparently have postingestional consequences that pro- Bufonids possess numerous bufodienolides (Flier et al.,
duce conditioned taste aversions (Masón et al., 1982). 1980; Habermehl, 1981), which are cardiotoxic steroids.
Noxious properties are far more widely distributed Some of these, such as bufotoxin and bufogenin, are
among amphibians than are toxins. Even the eggs of strictly cardiotoxic, whereas others have diverse effects.
some species have noxious properties^and those of Tar- A serotonin derivative, O-methyl-bufotenin, from Bu/o
icha, Atelopus, and at least some species of Bu/o contain alvarius, is a potent hallucinogen. Tetrodotoxin-like com-
toxins (see review by Brodie et al., 1978). Larger tad- pounds, zetekotoxin and chiriquitoxin, have been iso-
poles of some species (e.g., Rana chalconota, K. Liem, lated from the skins of Atelopus (Pavelka et al., 1977).
1961; Gastrophryne carolinensis, Cartón and Mushinsky, Dendrobatid frogs of the genus Dendrobates and espe-
1979) are unpalatable to predators presumably because cially Phyllobates have extremely toxic steroidal alkaloids
of the development of granular glands in late larval stages. in the skin (Daly et al., 1978; Myers and Daly, 1983).
Formanowicz and Brodie (1982) showed experimentally More than 200 alkaloids representing five distinct classes
that noxious qualities of several anurans and salamanders of compounds have been discovered in species of Den-
ECOLOGY
258

Figure 10-14. Aposematic

coloration ¡n amphibians:
predominantly red ¡n Pseudotriton
ruber from Ash Cave, Ohio (upper
left), and Dendrobatos pumilio from
the Río Changuinola, Panamá (upper
right); predominantly yellow in
Phyllobates terribilis from the upper
Río Saija drainage, Colombia
(middle left) and Atetopus zeteki from
El Copé, Panamá (middle right);
contrasting patterns of yellow and
black in Salamandra salamandra
from Europe (lower left) and orange-
red and dark brown in D. histrionicus
from El Valle, Chocó, Colombia
(lower right). Photos of anurans by
C. W. Myers, of salamanders by
W. E. Duellman.

drobates and Phyllobates, all of which have aposematic sand 20-gram whiíe mice, extrapolated lo be sufficierr
coloration. The molecular structure of the large majority lo kill several adulí humans (Myers el al., 1978).
of dendrobatid alkaloids consists of a simple piperidine The other dendrobaüd toxins are simpler in structure
ring of one nitrogen atom and five carbón atoms; piper- and much less toxic. Histrionicotoxins, firsl isolaled frc*»
idine rings occur in all groups of toxic dendrobatids. Dendrobates histrionicus, inleract with acetylcholine re-
However, in Phyllobates the biosynthesis of piperidine ceplors and block íhe transmission of signáis from nerves
alkaloids has been suppressed in favor of batrachotoxins, lo muscles and also block potassium channels in cel
which are extraordinarily toxic alkaloids. membranes. Pumilioloxin-B, flrst isolated from D. pum-
Batrachotoxins are among the most potent, naturally ilio, affecte the transport of calcium ions. Pumiliotoxin-C
occurring, nonprotein toxins. These compounds selec- and gephyrotoxin also block ions and prevent acetylcho-
üvely increase the permeability of the outer membranes line from triggering muscle contracüon. Lillle is knovw
of nerve and muscle fibers. Batrachotoxin prevenís the aboul self-immunity to these toxins. In Phyllobates ter-
normal closing of sodium channels in the cell membranes ribilis, a sodium-channel regulatory site in nerve and músete
with the result that cells become depolarized because of seems lo have been allered minimally, so that these frogs
massive influxes of sodium. Thus, nerve cells cannot are insensitivo to their own toxins bul nol lo similariy
transmit impulses, and muscle cells remain in an acti- acting plañí toxins, to which they are never exposed in
vated, contracled state. This resulte in heart arrhythmias, nalure (Daly el al., 1980).
fibrillation, and failure. An individual of the largest species
of highly toxic dendrobatíd, Phyllobates terribilis, (Fig. Aposematic Coloration. Amphibians that have toxic
10-14) contains enough toxin ío kill about twenty thou- skin secretions lend lo have aposematic colors or par-
 Enemies and Defense
2ms. These so-called warning colors supposedly func- Several examples of Batesian mimicry (noxious model 259
ión in providing visual warning, a learned response on and palatable mimic) are known among North American
±ie part of the predator. For this reason, noxious qualities salamanders. The red phase of Plethodon cinereus is a
presumably are associated with toxic propertíes, although mimic of the toxic eft stage of Notophthalmus virídescens
the former may be present without the latter. A predator (Brodie and Brodie, 1980). In parts of its range in the
iiat finds a certain kind of amphibian to be distasteful southem Appalachian Mountains, populations of the dis-
will associate the warning color with the bad taste and tasteful, black Plethodon jordani have red markings. In
after one or more such experiences will recognize the the área where P. jordani has red cheeks, some individ-
dstasteful species and refrain from artacking. uáis of the palatable Desmognathus imitator mimic this
Aposematic coloraüon usually involves red, orange, or pattern. In áreas where P. jordani has red legs, some
yellow. The animal may be predominantly or uniformly individuáis of D. ochrophaeus are mimeüc (R. R. Howard
one of these colors, such as Dendrobates pumi/io and and Brodie, 1973). In each of these cases, the mimics
Pseudotriton ruber (red), and Phyllobates terribilis and are polymorphic. Experimental feeding triáis of models,
Alelopus zetefci (yellow), or it may bear these colors against mimics, and nonmimic conspecifics resulted in signifi-
a contrasting background, usually black, as in Salaman- cantly higher survival of mimics than nonmimics.
dra salamandra and D. histrionicus (Fig. 10-14). In most The aposematic coloration of the toxic Pseudotriton
anurans and many salamanders, aposematic coloraüon was interpreted by Brandon and Huheey (1981) as a
is present on the dorsum; some salamanders and a few case of Müllerian mimicry with the coloration of the highly
anurans have aposemaüc coloratíon ventrally, and some toxic Notophthalmus viridescens. In this situation the ef-
of these exhibit the Unken posture in which the ventral fecüveness of the model is reinforced by the presence of
color is displayed. a toxic mimic. There is a size-correlated degree of toxicity
Some amphibians have striking patterns that may be in P. ruber; it is most toxic when it is the size of the efts
aposematic, but neither the presence of toxins ñor cor- of Notophthalmus, and its level of toxicity declines with
relative behavior has been observed. Included here are larger size.
the "bull's-eye" black and white ventral patterns in some
African Phrynobatrachus and the white spot on the brown
chest of some neotropical Phyllomedusa. EVOLUTION OF DEFENSE MECHANISMS
Among terrestrial vertebrales, amphibians are unique in
Mimicry. There are few examples of mimicry among possessing two kinds of integumentary glands: mucous
amphibians. The palatable Eleutherodactylus gaigeae has and granular. These glands produce at least two kinds of
a color pattern closely resembling the highly toxic Phyl- substances: mucus for maintaining a moist surface for
•obates aurotaenia and P. lugubris, with which it occurs cutaneous respiration and, in some species, toxins for
in sympatry (Myers and Daly, 1983) (Fig. 10-15). How- protection against predators. Basic similarities in the mor-
ever, there is no experimental evidence to support this phology of granular glands in diverse amphibians (see
presumed Batesian mimicry, or that of the presumably Chapter 14 and Neuwirth et al., 1979) suggest Ihat the
palatable Lithodytes lineatus and the slightly toxic Den- granular glands probably served an original function olher
drobates femoralis (C. Nelson and G. Miller, 1971). than poison synthesis, but the glands may have been a

Figure 10-15. Highly toxic model

Phyllobates lugubris from Isla Colón,
Panamá (left), and the Batesian
mimic Eleutherodactylus gaigeae
from the Río Concepción, Panamá
(right). Photos by C. W. Myers.
ECOLOGY
260 convenient preadaptation for producing the diverse tox- are subject to heavy predatíon (Wassersug and Sperry.
ins that evolved independentíy in several groups of am- 1977; Arnold and Wassersug, 1978), possibly not only
phibians. In fact, Flier et al. (1980) demonstrated that because of their inability to escape but also because of
various bufonids contain high levéis of compounds in the incomplete development of the granular glands.
skin that inhibit sodium- and potassium-dependent Tail autotomy is common among plethodontid sala-
adenosinetriphosphatase as well as the binding of oua- manders and also occurs in the salamandrid Chioglossa
bain to the enzyme; they hypothesized that the toxins in lusitanica— all of which have wound-healing properties.
bufonids may have originated from compounds that reg- Autotomy may have evolved independentíy in three dif-
úlate enzymes involved in maintaining salt and water bal- ferent ways among plethodontids, and D. Wake and
ance. Dresner (1967) suggested that selection has been for be-
As concluded for salamanders by Brodie (1983) and havior and structural adaptations for control of tail loss.
also emphasized in the preceding discussion, Skin Tox- rather than for tail loss per se. This suggestion is sup-
ins: Anurans, the basic factor underlying the evolution of ported by the tail undulatíon behavior of some pletho-
the various antipredator mechanisms is the distribution dontids and the attraction of predators to the tail, which
of granular glands on the body and the degree of de- not only is dispensable but also contains the highest con-
velopment of noxious or toxic secretíons of these glands. centratíon of granular glands. Salamanders that exhibir
Thus, there has been considerable convergence ¡n de- caudal autotomy lose the tail upon being grasped by a
fensive behavior in independen! lineages of anurans as predator; under these conditions salamanders that are
well as in salamanders, but some salamandrids and den- tailless at the time of an attack have a lower survival rate
drobaüds have developed highly toxic secretíons that are than those with a tail (Ducey and Brodie, 1983).
unique to trióse groups. These secretíons can be viewed There seems to be a relationship between aerobic and
as the ultímate in secretory defense mechanisms, which anaerobic capacities of amphibians on one hand and
are associated with aposematíc coloratíon. Many poten- , normal escape behavior on the other; species that rely
tial predators quickly learn to avoid these amphibians on burst activity for rapid escape utílize anaerobic me-
(R. R. Howard and Brodie, 1973; Hensel and Brodie, tabolism (A. Bennett and P. Licht, 1973; J. Baldwin et
1976). Even invertebrate predators (diving beetles, Dy- al., 1977). Amphibians that do not utilize burst activity
tiscus) and possibly parasitíc leeches learn to avoid the commonly have noxious or toxic secretions; thus, slow-
noxious skin secretíons of newts, Notophthalmus uirides- moving anurans (e.g., Bufo, Scaphiopus, Atelopus) and
cens (Pough, 1971; Brodie and Formanowicz, 1981). salamanders (e.g., Salamandra) that have high aerobic
Some predators, especially certain snakes, seem to be scopes rely on their noxious skin secretions to avoid pre-
immune to amphibian toxins. For example, colubrid snakes datíon. Anaerobic metabolism is associated with strug-
of the genera Heterodon and Xenodon feed almost ex- gling with a predator; in the salamander Plethodon jor-
clusively on Bu/o, adults of which are avoided by most dani, lactate concentratíons arising from anaerobic
other snakes. The colubrid Liophis epinephelus is im- metabolism during escape from snakes reached 880% oí
mune to a variety of potent toxins, even batrachotoxins, the resting level (Peder and Arnold, 1982).
for captíve snakes have fed on Atelopus, Dendrobates, Although almost any kind of predator may try to eai
and even the highly toxic Phyllobates terribilis with no an amphibian, amphibians are able to survive because
apparent ill effects (Myers et al., 1978). Thamnophis sir- they have evolved a diverse suite of antipredator mech-
talis is resistant to the strong toxins of Taricha and eats anisms. Morphological and metabolic features are cor-
the salamanders without apparent ill effects (Brodie, 1968). related with these mechanisms; aside from flight and con-
Although eggs and larvae of some amphibians have cealment, the basis for most defensive behavior is the
noxious or even toxic properties, these defense mecha- presence of granular glands, the diverse secretions of which
nisms develop in the metamorphic stages of some am- make many amphibians distasteful to predators.
phibians (Brodie et al., 1978). Metamorphosing anurans
 CHAPTER 11
The disparity between theory and
empiricism is particularly conspicuous in
anuran ecology and behavior, where
detailed studies of natural populations are
rare.
Population
Arnold G. Kluge (1981)
Biology

. opulations are made up of conspecific individuáis of and reproductive life span. Furthermore, absolute size is
different sexes, sizes, and age classes. Each individual has important with respect to fecundity (see Chapter 2). All
a history of growth and, upon reaching sexual maturity, of these factors are interrelated (Stearns, 1976).
reproduction. Characterisücs such as growth rates, size,
and longevity of individuáis are integral aspects of the Growth Rates
demographic features of populations. These factors, plus* Amphibians presumably have indeterminate growth. Most
movements, interactions with conspecific individuáis, and information on growth rates is for températe zone species
environmental constraints, constitute the main elements of anurans that have restricted growing seasons (Table
of population dynamics. 11-1). For example, the postmetamoiphic growth rate of
Although various aspects of population biology have the bullfrog Rana catesbeiana is rapid at early ages and
been studied in numerous species of amphibians, com- tends to level off with increased age (Fig. 11-1). Most
prehensive data are available for only a few species, and importantly for températe zone species, the time to reach
there have been no recent summaries or syntheses of adult size and to become sexually mature is a function
existing data. In this chapter, data on individual charac- not just of the growth rate but of the duration of the
terisücs, movements, and demography are summarized individual's seasonal activity period. F. Turner (1960a)
and synthesized with respect to the factors regulating summarized data on postmetamorphic growth in anu-
population densities. Material on the reproductive aspects rans, but there has been no equivalen! summary of sal-
of population biology is included in Chapter 2 {see espe- amanders;
cially Tables 2-6 through 2-9), whereas information on Geographic differences in growth rates probably are
larval growth and developmental périods is presented in influenced by differences in the physical environment.
Chapter 6. For example, bullfrogs (Rana catesbeiana) metamor-
phose at a mean length of 40 mm in Louisiana and grow
to a mean length of 69 mm before hibernating and to a
CHARACTERISTICS OF INDIVIDUALS mean length of 129 mm the next year; in New York the
Individuáis are the constituents of populations. Importan! frogs are larger at metamorphosis (mean = 45 mm) but
individual demographic characteristics include growth rate grow to only 53-55 mm before hibernating and to 93-100
and longevity, with the latter being especially importan! mm the next year (F. Turner, 1960a). A similar difference
with respect to the individual's age at first reproduction exists between populations of the slimy salamander
261
Table 11-1. Postmetamorphic Growth Rates of Températe Zone Anurans as Revealed by Studies of Natural Populaflons*

Mazlnium
siz e Age
Sizeat Sizeat
Species Male Female nletamorphosis hibernation lyt 2yr 3vr 4 yr Reference
Ascaphus truel 55 56 26 32 38 44 49 Daugherty and Sheldon (1982a)
Bambino bombina 56 56 17 22 35 45 — — Bannikov (1950)
Scaphiopus holbroofá 77 71 10 — 42 50 53 — P. Pearson (1955)
Bufo amerícanus 100 115 10 30 70 88 — — Hamilton (1934)
Bufo bufo 75 83 10 17 30 47 60 — Heusser (1970c)
Bufo quercicus 26 30 7 18 27 — — — Hamilton (1955)
Hyla regula 44 — 14 21 34 — — — Jameson (1956)
Rana catesbeiana — 155 45 53 93 123 138 — Raney and W. Ingram (1941)
Rana clamitans 103 105 32 38 66 83 89 — Martof (1956)
Rana pipiens 82 93 25 47 67 73 — — R. Ryan (1953)
Rana pretiosa 61 72 16 25 35 42 48 — F. Tumer (1957)
Gastrophryne olivácea 37 42 15 20 31 — — — Fitch (1956)
*A11 sizes are in millimeters for snout-vent length and represent mean or modal valúes.
 Population Biology
glutinosas) in Florida and Maryland (Houck, ing their first year. Rates of 14—18 mm during the first 263
15S2): in Florida the growth rate is about 21 mm the first year are known for three species of tropical plethodontíd
•ja:, compared to 16 mm in Maryland. salamanders (Houck, 1982). The most rapid growth rate
Similar patterns of growth rate are shown by several in a plethodontíd is by P. glutinosas in Florida, which
zerles of salamanders. For example, data on four spe- grows an average of 21 mm during the first year (High-
Des of Plethodon summarized by Peacock and Nuss- ton, 1956). Juvenile P. jordani do not appear above-
baum (1973) show that 28-33% of posthatching growth ground until they are 1 year oíd; during their second year,
zerars during the first year; in these small salamanders average growth in snout-vent length is 13.92 mm, whereas
fe rate of growth is 10—15 mm (snout-vent length) dur- during the next season of activity average growth is 9.26
mm and growth rate declines in subsequent years (Hair-
ston, 1983a). Growth rates of newts are comparable to
those of plethodonüds; most growth occurs during the
250 terrestrial eft stage in Trituras vulgaris (G. Bell, 1977; Fig.
11-2) and Notophthalmus viridescens (Gilí, 1978). In the
White River of Missouri, U.S.A., the hellbender (Cryp-
200- tobranchus alleganiensis) adds about 68 mm to total length
during the first year after metamorphosis to a length of
125 mm; large adults ( 400 mm) grow at a rate of about
'50- 1 mm per year (Peterson et al., 1983).
Many tropical anurans apparently grow throughout the
year and thus attain their adult sizes rapidly. Data on
introduced populaüons of the toad Bufo marinas indícate
'00- extremely rapid growth. In Hawaii, metamorphosing young
of 8-12 mm attain lengths of 60-75 mm in 3 months
and 90-120 mm at the age of 6 months (Pemberton,
50- 1934). The large neotropical tree frog, Hyla rosenbergi,
grows at a rate of 0.21 mm per day and reaches adult
size in less than 1 year (Kluge, 1981). The growth rates
0- of the tropical Rana erythraea in the Philippines is much
more rapid than that of températe species (W. Brown
Metamorphosis 1 2 3 4
and Alcalá, 1970). Pernales grow about 11 mm during
Years
the first month after metamorphosis, reach 76-83% of
Figure 11-1. Growth curve for the bullfrog Rana catesbeiana ¡n their máximum size in 1 year, and maintain a growth rate
Knois. The points are average weights of marked frogs of known of about 1 mm per month after about 7 months of age.
ages in a natural population. Data from Durham and G. Bennett
1963). Males grow about 6 mm during the first month after

40
Juveniles Adults

-48 I

-46

- 30-I
-44

~ 25- 1-42
I

i 2o^ -40 |

-38 Figure 11-2. Growth curves for juvenile

(terrestrial) and adult stages of the newt Triturus
5 6 7 uulgaris. The points are average lengths of
10 11 cohorts in a natural population. Adapted from
Years G. Bell (1977).
ECOLOGY
264 metamorphosis, reach 96% of their máximum size in 1 Caecilia exceed 1 m in total length; the largest known
year, and maintain a growth rate of about 1 mm per caecilian is a C. thompsoni having a length of 1515 mm.
month after 6 or 7 months of age. These growth rates The smallest caecilians are the West African /diocraníum
are comparable to those of three Bornean species of ffana russeli and the Seychellean Grandisonia breuis, which
reported by Inger and Greenberg (1966). Growth to sex- attain lengths of only 114 and 112 mm, respecüvely; a
ual maturity within the first year is the rule in tropical female of the former was sexually mature at a length of
anurans and also occurs in some températe zone species only 90 mm (E. Taylor, 1968).
(see Table 2-9). The giant Asiatic salamanders of the genus Ananas are
Few data on growth rates of caecilians are available. the largest living salamanders. Andríos davidianus attains
M. Wake's (1980b) analysis of a populatíon of Dermo- a total length of 1520 mm, and A. japonicus attains a
phis mexicanus in Guatemala showed that newly born total length of 1440 mm, much larger than the next larg-
individuáis have lengths of 108-155 mm and that the est salamanders—Amphiuma tridactylum (1015 mm) and
smallest reproductive females are 2 years oíd and have Siren lacertina (950 mm). A living Andrias japonicus hav-
lengths of 320-335 mm; thus, this caecilian grows at a ing a length of 1440 mm weighed 40 kg (Flower, 1936).
rate of nearly 100 mm per year for the first 2 years. The smallest salamanders are members of the pletho-
Determination of age classes in a sample of Geotrypetes dontid genus Thorius. In an unnamed species of Thorius
seraphini from Ghana by M. Wake (1977a) implies rapid from Cerro Pelón, Oaxaca, México, the smallest sexually
rates of growth; newly born individuáis have lengths of mature male has a snout-vent length of 15.7 mm and a
70-81 mm, whereas at the age of 2 years the caecilians total length of 26.9 mm (J. Hanken, pers. comm.).
are 180-240 mm long. The largest anuran is the West African ranid Conraua
Many factors affect growth rates, including the avail- goliath with a snout-vent length of 300 mm and a weight
ability of an abundance of essential food. However, dif- up to 3.3 kg. This immense size is approached (but not
ferent food Ítems vary in their quality (caloñe contení and very closely) by the South American Bu/o blombergi,
digesübility), so that the kinds of prey eaten (Fig. 11-3A), which reaches 250 mm, and by Bu/o marinus in the
the efficiency of capture rates, and energy used in cap- Guianan región of South America; there, the toads attain
turing prey all potentially contribute to the growth rate snout-vent lengths of 240 mm. The smallest anurans are
(see Chapter 12). Moreover, abiotic factors may influ- the Brazilian brachycephalid Psyllophryne didáctila (the
ence growth rate, especially among young amphibians. most diminuüve known tetrapod) reaching only 9.8 mm
For example, Lillywhite et al. (1973) suggested that be- in snout-vent length and the Cuban leptodactylid Smin-
havioral thermoregulation in young Bu/o bóreas was im- thillus limbatus attaining a length of 11.5 mm.
portant in raising body temperatures to increase digestive
rates. C. Richards and Lehman (1980) demonstrated that Longevity
constant light has a positíve effect on growth rates of Little is known about the longevity of amphibians in na-
postmetamorphic Rana pipiens (Fig. 11-3B). The results ture. On the basis of records of captive individuáis, it is
of these laboratory studies need to be incorporated into evident that many kinds of amphibians have the potenüal
investigations of growth rates in natural populaüons. to live for two or more decades (Table 11-2). Generally.
the longest-lived amphibians are the large aquatic sala-
Size manders, although a record of 50 years for a Salamandra
There ¡s great disparity in the máximum sizes attained by salamandra (Bohme, 1979) approaches the record of 55
different species in the three living orders of amphibians. years for Andrias japonicus. Moreover, it seems that larger
Several species of caecilians in the South American genus species tend to live longer than smaller ones, and that

Figure 11-3. Growth rates of

recently metamorphosed anurans.
A. Effects of diet on Bu/o 7- -28
woodhousii. Curve 1 = diet of
crickets (Acheta domestica); 2 =
diet of cabbage loopers (Trichoplusia
sp.); 3 = diet of mealworms 5-
(Tenebrio motitor); 4 = combined ro
diet. The points are mean weights of -5 Ó
15 toads in each group. Adapted 3- " -12
from Claussen and Layne (1983).
B. Effects of photoperiod on Rana
pipiens. Solid line = constant light;
broken line = 8 hours of light per 1- -4
day. The points are mean weights for
13 individuáis at 21 weeks and 40
individuáis at the beginning. Adapted 2 4 6 8 O 3 6 9 12 15 18 21
from C. Richards and Lehman (1980). Weeks
 Populatíon Biology
salamanders are longer-lived than anurans. The corre- Table 11-2. Selected Longevity Records for Captive Amphibians* 265
lation with size may be an artifact because zoos tend to Species Age (years)
maintain larger species for display. Nonetheless, in nature
larger amphibians probably are less prone to predaüon Caecilians
Typhlonectes compressicauda
than smaller ones and therefore might have a greater life
expectancy, but because larger individuáis require more Salamanders
food, their life expectancy or fitness might be reduced. Hynobius bou/engeri 5
Notable discrepancies exist between longevity records Andrios japónicas 55
in captivity and life expectancy in nature. For example, Cryptobranchus alleganiensis 55
Siren lacertina 25
Bowler (1977) reported that five adult male Hy/a rosen- Necturus maculosus 9
bergi lived for 3.5 years in captivity, but Kluge (1981) Proteus anguinus 15
found no males that survived 2 years in nature. The records Cynops pyrrogaster 25
of 4—5 years for many plethodontid salamanders in cap- Pleurodeles waltl 20
Salamandra salamandra 50
tivity (Bowler, 1977) do not reflect the potenüal longevity Taricha torosa 21
of these salamanders in nature, because many of the Triturus vulgaris 28
species do not reach sexual maturity until they are 4 years Amphiuma means 27
of age (see Chapter 2). On the other hand, some estí- Ambystoma mexicanum 25
Various plethodontids 5
males of age of individuáis in nature correspond well with
longevity records for captive individuáis; for example, Pe- Anurans
terson et al. (1983) estimated the largest individuáis in a Xenopus laevis 15
populatíon of Cryptobranchus alleganiensis to be 25 years Bombina bambino 20
oíd, only 4 years less than the record for a captive (Flower, Scaphiopus holbrooki 12
Ceratophrys ornato 13
1936). Leptodactylus pentadactylus 15
Bufo bufo 36
Dendrobates auratus 8
MOVEMENTS AND TERRITORIALITY Hy/a arbórea 14
Litaría caerutea 16
Movement patterns of individuáis are fundamental com- Osteopilus septentríonalis 13
ponents of the ecology and populatíon biology of a spe- Rana catesbeiana 16
cies. Movement patterns probably reflect age-specific Kaloula pulchra 6
variation in life history strategies with subsequent differ-
*Based mainly on Flower (1936) and Bowler (1977).
ences in ecological requirements. Among amphibians,
migrations are associated mostly with reproductíve ag-
gregations (see Chapter 3), but dispersión of recently ing sites; reproduction occurs within the home ranges of
metamorphosed young also may involve movements over terrestrial amphibians such as eleutherodactyline frogs and
long distances. Young of Bufo marinas move about 150 plethodontine salamanders.
m away from their natal ponds (G. Zug and P. Zug, Home range requirements differ among species, but
1979), and young of Hy/a regula move up to 237 m from shelter and food are mandatory components. The home
a natal pond (Jameson, 1956). The young of Syrrhophus range usually encompasses a preferred shelter and one
marnocki move 112 to 300 m (mean = 211 m) from or more feeding sites, and, for many kinds of male anu-
their terrestrial nest sites before establishing residency rans it may include a suitable calling site.
(Jameson, 1955a). For amphibians, the sizes of home ranges generally can
Movements of individuáis have been ascertained by be correlated with the size of the animal. For example,
capture-recapture studies of animáis that have been G. Zug and P. Zug (1979) determined the average size
marked by toe-clipping, branding, tags, or dyes. Move- of the foraging área (as a main componen! of the home
ments of individuáis can be monitored more accurately range) to be 160 m2 in the large toad Bufo marinus on
when the animáis have been tagged with radioactive iso- Barro Colorado Island, Panamá. The home range of Rana
topes, because then continuous monitoring of individuáis c/amitans is 20 to 200 m2 (mean = 60 m2) (Martof, 1953)
provides an hour-by-hour or day-by-day schedule of and that of Leptodactylus macrostemum, 9.4 to 134 m2
movements, whereas most capture-recapture studies do (Dixon and Staton, 1976). In the terrestrial, montane
not provide such accuracy. bufonid Atelopus oxyrhynchus, home ranges are larger
in males (mean = 56.2 m2) than females (32.6 m2) (Dole
Home Range and Durant, 1974a). Males of the small Dendrobates
Home range is considered to be the área in which an pumi/io have home ranges of only 20 m2 (McVey et al.,
individual carnes out its normal daily activities. Migrations 1981). However, Syrrhophus mamocki is an exception;
to breeding sites outside the área of daily activity should Jameson (1955a) calculated the size of the home ranges
not be considered to occur within the home range. How- of this relatívely small terrestrial leptodactylid to vary from
ever, many kinds of amphibians do not migrate to breed- 267 to 700 m2.
ECOLOGY
Among salamanders, Ambystoma macu/atum have calling sites along streams at night and back to diurnal
home ranges of 3.3 to 29.4 m2 (mean = 9.83 m2) (Klee- perches by day have a third dimensión to their home
berger and J. Werner, 1983); in Salamandra salamandra, ranges, but these have not been measured.
the average home range of males is 9.8 m2 and of fe- Many other studies have provided information on dis-
males 12.8 m2 (Degani and Warburg, 1978). The sizes tances moved by amphibians during their daily activities.
of home ranges among terrestrial plethodonüd salaman- but they have not quantified home ranges as such. These
ders vary greatly. For example, in Ensatina eschscholtzi, data suggest that the home ranges of some amphibians
the average home range of males is 1194 rn2 and of may be greater than those already mentioned. For ex-
females only 314 m2 (Stebbins, 1951). In contras!, male ample, Heusser (1968) noted that Bufo bufo forages for
Plethodon cinereus have smaller home ranges distances of 50 to 150 m, and Pyburn (1958) reported
(mean = 10.8 m2) than females (mean = 19.9 m2) that Acris crepitans move 15 to 100 m along the margin
(Kleeberger and J. Werner, 1982). Representativo sizes of a pond. Some amphibians may not have definable
of home ranges in other terrestrial plethodontids in which home ranges, but instead move about arbitrarily in fa-
there are no significant differences between the sexes are: vorable habitat, as in Notophthalmus viridescens (R. N.
Batrachoseps attenuatus, 7.1 m2 (Hendrickson, 1954); Harris, 1981).
Bolitoglossa subpalmata, 44 m2 (Vial, 1968); Plethodon
glutinosas, 34 to 75 m2 (Merchant, 1972); and P. jordani, Homing Behavior
6.7 to 55 m2 (Madison and Shoop, 1970). In response to reduced food supply, lack of available
The shape of the home range obviously depends on shelter, or lack of mates, individuáis may extend or shift
the habitat of the animal. Although not defined formally, their home ranges. The ability to return to the home
shapes of home ranges have been described as linear, range is defined as homing behavior, and it provides a
two-dimensional, or three-dimensional. These are gen- means for returning to known haunts from breeding ac-
eralized and, at the best, loóse descriptive terms. Linear tivities or other searches. Moreover, in species that attend
is understood to be a point-to-point distribution, whereas their eggs, the ability to return to the nest site is importan!
a two-dimensional home range can be construed as an for the survival of the eggs. Some species use visual cues
animal's distribution in a planar space (e.g., surface of to lócate specific sites, whereas olfactory cues seem to be
the forest floor). A three-dimensional home range implies the primary stimuli for salamanders (see Chapter 3).
that the organism is active in more than one plañe; for Many species exhibit a high degree of fidelity to their
example, salamanders may utilize the forest floor by day home range; in fact, some long-distance displacements
and arboreal perches at night. have resulted in individuáis returning to exactly the same
Most terrestrial salamanders and anurans have planar place where they had been living. For example, individ-
ranges, but many salamanders descend below the sur- uáis of Bufo bufo displaced 3 km retumed to their home
face in times of drought; little attention has been paid to sites (Heusser, 1969), and newts, lancha rtvularis, that
this third dimensional component of home ranges. Using were displaced 8 km retumed to their home stream within
radioisotopes, Semlitsch (1981) tracked individual Am- 1 year (Twitty et al., 1967). Terrestrial plethodontids can
bystoma talpoideum in the underground burrows that return to their home ranges when displaced for modérate
consütute their summer home ranges; he found that within distances. For example, Plethodon jordani retumed when
their home ranges each individual had several activity displaced up to 150 m (Madison, 1969); 90% of P. ci-
centers with áreas from 0.02 to 0.21 m2. On the other nereus displaced 30 m returned to their home sites, but
hand, the home ranges of stream-inhabiting amphibians only 25% of those displaced 90 m returned (Kleeberger
usually are linear, as shown in Desmognathus fuscas by and J. Werner, 1982). Of 83 tree frogs, Hyla regilla.
Ashton (1975), who found that individuáis move 0.3 to which were displaced 275 m from a breeding site, 43
10.2 m (mean = 0.49 m) along a small stream, and in (76%) of 56 recovered frogs returned to the site within
D. ochrophaeus by Holomuzki (1982), who determined 1 month, but none of 414 frogs that was moved 914 m
that the average linear movement was 0.71 m. During to another pond returned to the original site within 1
the period of summer activity, adults of the stream-breed- month (Jameson, 1957).
ing tree frog Hyla cadaverina move only 1 to 5 m away Both European newts, Triturus vulgaris, and American
from the stream, and juveniles are even more sedentary, newts, Notophthalmus viridescens, have high fidelities to
moving only 0.5 to 2 m away (R. T. Harris, 1975). Bom- their breeding ponds; although these newts move about
bina variegata move more than 200 m to a breeding arbitrarily in the terrestrial environment, they usually re-
stream in the Balkan Mountains in Bulgaria, and during tum to the same ponds to breed (G. Bell, 1977; GilL
the breeding season, males move an average of 63.8 m 1978). Colonization of new ponds and formation of new
and females only 20.0 m along the stream (Beshkov and demes in a metapopulation of Notophthalmus is de-
Jameson, 1980). Likewise, the stream-inhabiting frog As- pendent on the dispersa! of efts (Gilí, 1978).
caphus tmei has linear home ranges (Daugherty and In prairies in Minnesota, Bufo hemiophrys breeds in
Sheldon, 1982b). Arboreal frogs that move vertically to shallow ponds, and there is no evidence of fidelity to
 Population Biology
rcular ponds by the toads; however 88 to 95% of the sites (Drewry, 1970). Defense of shelters against conspe- 267
f return to the same mound for hibernation in suc- cifics possibly is widespread in anurans; such behavior
years (Kelleher and Tester, 1969). has been reported in the defense of burrows by the Mex-
ican hylid Pachymedusa dacnicolor (Wiewandt, 1971)
Territoriality and several species of Pseudophryne in Australia (Pen-
isause territoriality is best understood in the context of gilley, 1971). Defense of feeding sites probably is much
zarpetitíon for limited resources, a territory can be de- more common than reported in the literatee, because
tec as an área coincident with, or included within, the many anurans (e.g., Eleutherodactylus and Centro/e-
TOTA range that is defended against intruders. Territo- nella) use the same perch for calling and feeding (also
stifcy is best understood in the context of compeütion for for oviposition by some species); thus, the defense of that
iored resources. Fidelity to, and defense of, a particular resource can be for several reasons.
S£ s advantageous if it provides the occupant exclusive, With the exception of the few observed cases of size-
arrrority, access to resources needed for the individual' s related dominance in defense of territories, there is little
sjr.rval or reproduction. Aggressive behavior related to evidence of hierarchical behavior in amphibians. Studies
siE-specific territoriality has been reported for numerous on captive anurans have produced conflicting results. Tracy
«res of amphibians. Most of these observaüons relate to (1973) noted a feeding hierarchy among young Bu/o
=xrship (see Chapter 3), and vocalization is an imper- bóreas but was unable to ascertain aggression. Boice and
ar: aspect of territoriality in many anurans (see Chapter Witter (1969) commented that there was no linear dom-
4. Aggressive defense of territories also is associated with inance in a feeding hierarchy of Rana pipiens. Haubrich
ajr.e kinds of parental care, especially among terrestrial (1961) concluded that in Xenopus laevis there were no
aetr.odontid salamanders and anurans that guard their absolute displays of dominance of one individual over
ages (see Chapter 2). As yet, there is no evidence that another in groups of individuáis, but in experiments with
•cae amphibians defend territories that include female various pairs definite aggression and dominance were
tarems and their offspring, as is the case in some lizards observed. It is unknown if aggressive intraspecific domi-
3C.á mammals. nance occurs in nature, and if so, whether such behavior
Laboratory observations by Thurow (1976) demon- may be related to the abundance of food, density of
srated that intraspecific social dominance occurred in conspecifics, or other factors.
«•.eral salamanders of the genus P/ethodon. Although
weniles interacted competitively among themselves, a
srong, size-related dominance exists, so that in contests
3er.veen individuáis of different sizes the larger animal DEMOGRAPHY
•on 22% of the time; in most of the other contests there In nearly all amphibian populations that have been stud-
•as no clear winner. R. Jaeger and Gergits (1979) showed ied, predation pressure on eggs and larvae is high, and
tat P. cinéreas mark their territories by pheromones and juvenile mortality vanes more than adult mortality. Un-
tat neighboring individuáis recognize each other's pher- predictable environmental conditions, such as a drought-
imones. In a series of laboratory experiments, R. Jaeger related disappearance of ponds, would affect survivor-
I981b) showed that adult male and female P. cinereus ship of eggs and larvae more than adults. Survivorship
sr.ployed "dear enemy" recognition. Individuáis were of eggs and larvae also may be correlated with the amount
jess aggressive and more submissive toward familiar ter- and kind of parental care, if any. Thus, determination of
rrorial neighbors than toward strangers, and pheromones demographic parameters, such as fecundity, natality, re-
were used to distinguish familiar from unfamiliar individ- cruitment, age at first reproduction, reproductive life span,
uáis. R. Jaeger concluded that this behavior reduces the and age-specific mortality, are contingent on density-
Ikelihood of escalated aggressive contests between independent factors such as environmental stability and
neighbors. When combat occurs, bites usually are di- mode of life history, including parental care, as well as
rected at two vulnerable parts of the body—the tail, which the usual density-dependent factors—available resources
ran lead to caudal autonomy and therefore loss of fat for shelter, oviposition sites, and sufficient food to main-
reserves, or the nasolabial grooves, scarring of which im- tain a positive energy budget.
pairs their chemosensory function, which results in a re- Fecundity and natality have been discussed with re-
áuced prey-capture rate during foraging and possibly re- spect to reproductive modes and parental care in Chapter
áuced ability to lócate mates and to defend a territory. 2. The other demographic parameters as they relate to
Many terrestrial dendrobatid frogs defend all-purpose the population dynamics of larval and postmetamorphic
territories that include feeding sites, calling sites, shelter, amphibians are treated here.
and oviposition sites (Wells, 1977a). Both males and fe-
males of Eleutherodacfylus coqui defend tree holes that Survivorship
are used as diurnal shelters and may be used as ovipo- Most of the published data on survivorship is obfuscated
sition sites, and at least some females defend their feeding by diverse methodologies that tend to make a synthesis
ECOLOGY
268 Table 11-3. Survivorship of Amphibian Eggs and Larvae
Percent survival
Eggs and
Species Eggs Larvae larvae Reference
Salamanders
Triturus uu/garis 2.6 8.8 0.23 G. Bell and Lawton (1975)
Ambystoma macu/afum 22.2 71.2 15.80 Shoop (1974)
Ambystoma tigrinum — — 3.30 J. Anderson et al. (1971)

Anurans
Rana aurora 91.0 5.3 4.82 L. Licht (1974)
Rana pretiosa 71.0 7.3 5.18 L Licht (1974)
Rana sy/uatica — — 4.00 Herrad and Kinney (1966)

difficult. Consequently, the following selected data are numbers of eggs, but survivorship must be much greater
summarized so as to provide a range of variation of sur- in order to maintain population sizes in those species that
vivorship of different stages in the life histories of various produce few offspring (e.g., terrestrial plethodonüd sal-
kinds of amphibians. amanders and dendrobatid frogs).
Survivorship of adult newts from their first to their sec-
Eggs. Survivorship of aquatic eggs to hatching ranges ond breeding year is about 50%, but the percentage dif-
from a low of 2.6% in Triturus vulgaris to a high of 91% fers between sexes. In Notophthalmus viridescens, the
in Rana aurora (Table 11-3). In the nest-building gladi- rate of survival of males is 51%, of females 43% (GilL
ator frog, Hyla rosenbergi, only 24% of 49 nests suffered 1978), whereas in Triturus vulgaris the rates are 45% for
little or no mortality, and no eggs survived in 22% of the males and 55% for females (G. Bell, 1977). Presumably
nests (Kluge, 1981); survivorship of eggs to hatching was the bright courtship colors of male T. vulgaris result in
only about 48%. In the arboreal foam nests of Po/yped- higher rates of predation than on females, even though
ates leucomystax, survivorship of eggs is O to 100% these newts have noxious skin secretions.
(mean = 34%) (Yorke, 1983). Terrestrial eggs, espe- Annual adult survivorship among anurans varíes from
cially with parental care, have greater survivorship; for O to 69% (Table 11-4). Limited data suggest that surviv-
example, more than 95% of the eggs survive to hatching orship is much lower in the tropics than in températe
in three species of Pseudophryne (Woodruff, 1976). regions. Of course, in the humid tropics the frogs are
active throughout the year and thus are susceptible to
Larvae. The survivorship of most larvae is rather low continuous predation pressure, whereas in many tem-
(Table 11-3), although there are some excepüons, espe- pérate species the season of activity is 6 months or less
cially among stream-inhabiting salamander larvae. Nuss- each year. In Hyla rosenbergi, the average length of resi-
baum and Clothier (1973) calculated that 43% of Di- dency in the breeding population is only 18.3 days for
camptodon ensaíus survive their first year of larval life; males and 23.2 days for females; only 3 of 109 markec
this survival rate is similar to those determined for the females returned to breed a second year, and none of
stream larvae of Ranodon sibiricus (42.7%; Bannikov, 178 males returned. Therefore, Kluge (1981) concludec
1949) and Pseudotriton ruber (50%; Bruce, 1972b). that annual population turnover was nearly 100%.
Survivorship of Rana larvae in ponds generally is less Survivorship of températe salamanders ranges from
than 10%. Calef (1973) found that there is higher mor- intermedíate between the extremes calculated for anu-
tality among tadpoles of Rana aurora during the first 4 rans to much greater than that of anurans. In the mos:
weeks after hatching; then mortality gradually declines, comprehensive study of survivorship, Organ (1961) cal-
so that only 5% survive to metamorphosis 11 to 14 weeks culated life tables for five species of Desmognathus and
after hatching. In contras!, 11.8 to 17.6% of the tadpoles showed that there is a progressive increase in early sur-
of Rana catesbeiana survive to metamorphosis (Cecil and vival rate from the most aquatic species, D. quadramac-
Just, 1979). u/atus, to the most terrestrial, D. wrighti (Table 11-5).
The annual survival rates of these salamanders are ap-
Postmetamorphics. Little informatíon is available on proximated by those of Bolitoglossa subpalmata (2\%:
the numbers of metamorphosing young that survive to Vial, 1968) and Plethodon jordani (36% in the seconc
sexual maturity. G. Zug and P. Zug (1979) extrapolated year and 48% in the third year; Hairston, 1983a). On
that only about 0.5% of young Bufo marinus survive to the other hand, Bruce (1976) showed that annual sur-
sexual maturity; this rate of survivorship would still result vivorship in the epigean Eurycea neotenes is about 10%
in an expansión of population size. This may be the ap- in the first year; survivorship increases among older sal-
proximate survivorship in species that produce large amanders, particularly males.
 Populatíon Biology
T»ble 11-4. Annual Survivorship of Some Adult Anurans 269
Percent
Species Sex survival Reference
auto hemiophrys 3, 9 34 Kelleher and Tester (1969)
Bufo woodhousii ó" , 9 22 R. Clarke (1977)
rr.'.a rosenbergi <J 0 Kluge (1981)
rf.ía rosenbergi 9 3 Kluge (1981)
Baña aurora 3, 9 69 L Licht (1974)
~¿r.a cascadae c? 59 Briggs and Storm (1970)
Szra cascadae $ 46 Briggs and Storm (1970)
5na erythraea <S, $ 2-5 W. Brown and Alcalá (1970)
Í5zra pretiosa 5 45 L. Licht (1974)
ína pretiosa $ 67 L. Licht (1974)

TaMe 11-5. Life Tables of Five Species of Plethodonüd Salamanders are recruited in large numbers. Conversely, species that
a ne Genus Desmognathus Arranged from the Most AquaBc to the have long breeding seasons or highly variable larval pe-
Mea Tenestrial*
riods may recruit young into their populations during much
Percent survival of their activity seasons. Thus, températe anurans that
Species Males Pernales Age (years) have múltiple clutches and/or overwintering of some of
D quadramaculatus 100.00 100.00 0-1 the tadpoles, as well as many tropical anurans that breed
20.30 13.00 3-4 throughout the year, may have nearly continuous re-
3.75 5.30 5-6 cruitment. However, not all tropical anurans follow this
0.56 0.08 7-8 pattern. For example, Bu/o typhonius has a short breed-
0.14 0.01 9-10 ing season with a mass metamorphosis of young (Wells,
D montícola 100.00 100.00 0-1
21.40 14.00 3-4 1979). Many savanna-inhabitíng species have distinct
5.70 4.90 5-6 seasonal recruitment of young (e.g., species of Ptycha-
1.56 0.75 7-8 dena; Barbault and Trefaut Rodrigues, 1978). Likewise,
0.26 0.01 9-10 some salamanders having lengthy aquatíc larval periods
D fuscus 100.00 100.00 0-1
28.80 15.60 3-4 may recruit metamorphosing young into the population
11.40 3.40 5-6 at various times of the year; for example, recruitment of
1.90 0.24 7-8 young of the plethodontid Stereochilus marginatus oc-
0.14 0.01 9-10 curs from April through November (Bruce, 1971)
D ochrophaeus 100.00 100.00 0-1 Most evidence points to an initíal 1:1 sex raüo in am-
35.20 28.50 3-4
19.50 12.00 5-6 phibians, even though in most explosive breeders the
6.30 2.70 7-8 number of males is much greater than that of females at
0.67 0.05 9-10 any given time at breeding sites. However, in many cases
D. wrighti 100.00 100.00 0-1 this is owing to the fact that males tend to remain at the
62.00 47.00 3-4
51.00 20.00 5-6 breeding sites, whereas once females have spawned, they
4.25 3.50 7-8 leave. This apparently is not the case in Ambystoma mac-
0.43 0.12 9-10 u/atum, in which captures of adults entering and leaving
a breeding pond revealed a much higher percentage of
"Based on Organ (1961).
males during a period of 5 years (Husting, 1965). In
some amphibians, differences in age-specific mortality
Populatíon Structure between the sexes results in skewed sex ratios. For some
Populations generally are made up of individuáis of dif- unknown reason, survivorship is lower in females than in
ferent ages and sexes. The timing of recruitment of young males of the newt Notophthalmus viridescens, so al-
into the populaüon depends on the duratíon of the though the sex ratio is 1:1 in recruits, the breeding pop-
breeding season and variation in the length of the larval ulation consists of about two males for each female (Gilí,
period; the amount of recruitment depends on the effec- 1978). The opposite is true in Triturus vulgaris, in which
áve size of the breeding population and the survivorship age-specific mortality affects males more significantly, with
of the eggs and larvae. Thus, the recruitment of young the result that more older breeding adults are females
•ji populations of Rana syluatica is high for a short period (G. Bell, 1977). Also, in some anurans in which male
of üme in early summer, because the breeding season of survivorship is greater than females (e.g., Rana aurora;
that species lasts for only a few days. Likewise, in mid to Briggs and Storm, 1970), males outnumber females in
late summer, metamorphosing young of highly seasonal the breeding population, whereas the sex ratio is 1:1 in
breeders, such as Scapriiopus couchii and Bu/o bóreas, immatures.
ECOLOGY
270
50

25

Sept/Oct Nov/Dec Jan/Feb Mar/Apr May/Jun

75

o
i-/-»
-560
o.
£

0)
o

Figure 11-4. Population structure in I

amphibians. A. A plethodontid o-
salamander, Plethodon richmondi, in
eastern Tennessee, in which small Jul Oct Dec Feb Mar Apr May Jun Jul Aug
numbers of young are recruited into
the population over severa) months 75-
(data from Nagel, 1979). B. An
anuran, Eleutherodactylus caqui, in
humid forest in Puerto Rico, in which
young are recruited throughout most
of the year (data from Stewart and 50-
Pough, 1983). C. An anuran,
Ptychadena maccarthyensis, in the
seasonally wet savannas of the Ivory
Coast, in which young are recruited 25-
only after a short breeding season
(data from Barbault and Trefaut
Rodrigues, 1978). Heavy lines =
adults; light lines = subadults; solid
lines = males; broken lines = 0-
females; double lines = both sexes;
dashes-and-dots = juveniles. Jan Feb Mar Apr May Jun Jul Aug Sept Oct Nov Dec

By determining the numbers of individuáis in different out the year, the population always contains a high per-
size (age) classes, growth rates, and size or age at sexual centage of juveniles. However, in those species that have
maturity of each sex, it is possible to quanüfy the structure short breeding seasons, juveniles are absent during part
of populations. For example, among pond-breeding Rana, of the year but tend to make up a large percentage of
sexually mature frogs constituted 50.6% of the popula- the population after a period of metamorphosis (Fig. 11-
tion oiR. pretiosa in Wyoming (F. Tumer, 1960b), whereas 4). In the first case annual population turnover is low,
somewhat lower percentages prevailed in tropical species whereas in the last two examples population turnover
having year-round recruitment—47.7% in R. blythi, 47.0% may be modérate or approach 100%, depending on the
in R. macrodon, and 27.6% in R. ibanorum, all in Borneo survivorship of the adults.
(Inger and Greenberg, 1966), and 15 to 33% in R. er-
ythraea in the Philippines (W. Brown and Alcalá, 1970). Population Density
Some plethodontid salamanders are relaüvely long-lived Most studies of amphibian populations include informa-
and do not reach sexual maturity until they are at least tion on the size of the population only as total numbers
2 to 4 years oíd; furthermore, females produce relatívely without regard to área. Thus, actual densities are impos-
small numbers of young only biennially. At any given sible to determine from many of the data. Moreover,
time, populations of these species consist primarily of many studies involving species that aggregate for breed-
adults. In contrast, in species of tropical anurans in which ing include data only on the number of breeding individ-
the adult life span is short and breeding occurs through- uáis. These data are useful in determining the size of
 Population Biology
arecding congregations but provide no real idea of the There is great variation in the densities of local popu- 271
asnsity of the species throughout the habitat. lations of plethodontid salamanders (Table 11-6). Sev-
As examples, Husting's (1965) study of Ambystoma eral populaüon estimates are available for Plethodon ci-
naculatum revealed the presence of 234 to 315 males nereus (see T. M. Burton and Likens, 1975, for references).
ird 69 to 155 females annually for each of 5 years in a A surface census in Michigan provided an estímate of
3cnd with an área of about 1,250 m2 in Michigan. In 0.0496/m2, whereas digging up of plots of dry and wet
Bch of five ponds of about 150 m2 área in the mountains litter resulted in estimates of 0.0900 and 0.8900/m2, re-
oí Virginia, Gilí (1978) found breeding populations of spectively. Mark-recapture data from Pennsylvania pro-
\otophthalmus viridescens during a period of 3 years to vided an estímate of 0.2118/m2, and a surface census
be as low as 6 to 44 (mean = 25) in one pond and as after a rain in Virginia gave an estímate of 0.210 to 0.250/
kgh as 1867 to 2637 (mean = 2195) in another. In m2. R. Jaeger (1980c) estimated a surface density of 2.2/
Costa Rica, the tree frog Agalychnis spurrelli was found m2 in Virginia; density did not vary significantly over 22
rreeding in incredible numbers; N. Scott and A. Starrett days of sampling. Salamander densities in a forest in New
(1974) estimated about 200 frogs per meter of shoreline Hampshire are extremely high; T. M. Burton and Likens
sround a pond of about 3500 m2 área and estimated a (1975) estimated that populations of four species (Des-
T>al of 13,000 frogs in the pond on one night. Gadow mognathus ochrophaeus, Eurycea bislineata, Gyrinophi-
1908) estimated a minimum of 45,000 tree frogs (Smi- lus porphyriticus, and Plethodon cinereus) consisted of
Éca baudinii) in a pond of about 750 m2 in southern 106,508 individuáis in 36.1 hectares. Of these, P. cinere-
Veracruz, México. us comprised 93.5% with 95,000 individuáis having a
The most meaningful estimates of densities of anurans biomass of 59.85 kg (1.65 kg/ha). These estimates are
are from censuses taken when the animáis are not breed- even more impressive when compared to those of other
rg or of species that do not congrégate for breeding. For groups of animáis in the same forest; not only are there
ctample, seven species of Eleutherodactylus inhabiüng more salamanders than all birds and mammals com-
doud forest leaf litter at San Vito, Costa Rica, have den- bined, but the biomass of salamanders is 2.6 times higher
snes of 0.0017 to 0.459/m2 (mean = 0.0775/m2), but (wet weight) than that of birds during the peak of the
r.e most abundan! of these, E. stejnegerianus, has a den- breeding season and is about equal to that of shrews and
scy of only 0.043/m2 in the Osa Península of Costa Rica mice combined.
N. Scott, 1976). Estimated densities of other terrestrial Population densities are dependent on many factors,
iogs range from 0.00029/m2 for Syrrhophus mamocki such as available resources or variation in predator pres-
TÍ Texas (Jameson, 1955a) to 0.010/m2 for Eleuthero- sure. Thus, the two- to fivefold increase in densities of
dactylus lynchi and 0.016/m2 for Atelopus ebenoides in Batrachoseps attenuatus on islands in San Francisco Bay
a páramo in the Colombian Andes, and 0.0152/m2 for over those on the mainland (P. K. Anderson, 1960) may
Pleurodema mamnorata on the Altiplano of Bolivia (Pé- be the result of lower predation pressure on the islands.
áur and Duellman, 1980). The highest densities have Differences in densities may be owing to local microen-
been reported for the bufonid Nectophrynoides occiden- vironmental conditions (e.g., Plethodon cinereus) or time
23ÍÍS on Mont Nimba in West África, where on one date of the year (e.g., Nectophrynoides occidentalis). Minor
iie total density was 5.92/m2 (1.64/m2 for adults and differences in habitat may affect densities; for example,
4.28/m2 for juveniles) and at another time, 4.72 adults/ in New Guinea, Bu/o marinus occurs in densities of 0.0001
m2 (Lamotte, 1959). to 0.0003/m2 in undisturbed savannas and 0.0030/m2 in

Tibie 11-6. Estimated Densities of Populations of Plethodontid Salamanders

Species Individnals/m2 Reference
Aneides aeneus 0.2500-0.1000 R. Cordón (1952)
Aneides lugubris 0.4051-0.4989° P. K. Anderson (1960)
Batrachoseps attenuatus 0.4516 Hendrickson (1954)
Batrachoseps attenuatus 0.9500-2.0155° P. K. Anderson (1960)
Bolitoglossa subpalmata 0.7560-0.9097 Vial (1968)
Desmognathus fuscus 0.4000-1.4000 Spight (1967b)
Desmognathus ochrophaeus 0.0170 R. Cordón et al. (1962)
Ensatina eschscholtzí 0.1482-0.1729 Stebbins (1954)
Plethodon cinereus 0.0496" Test and Bingham (1948)
Plethodon cinereus 2.3670-2.5830" T. M. Burton and Likens
(1975)
Plethodon glutinosus 0.0040 R. Cordón et al. (1962)
Plethodon glutinosus 0.4180-0.8440 Semlitsch (1980)
Plethodon jordani 0.0220 R. Cordón et al. (1962)
Plethodon yonahlossee 0.0070 R. Cordón et al. (1962)
^land populations.
Extremes of esfimates from Michigan and New Hampshire; other estimates are intermedíate (see text).
ECOLOGY
* ** the vicinity of human habitation, where food presumably rufitela on Barro Colorado Island, Panamá, remained more
is more abundant (G. Zug et al., 1975). The habitat of or less constant and confined to one or two breeding
Eleutherodactylus coqui in Puerto Rico was altered ex- sites for nearly 50 years; the population expanded greatly
perimentally by placing bamboo retreats in some study and dispersed over much of the island in 1980, possibly
plots; after 1 year the experimental plots contained sig- as a result of favorable conditions (short dry season) in
nificantly more frogs than did the control plots (Stewart 1979-80 (Rand et al., 1983).
and Pough, 1983). The highest reported density of an Variable climatic conditions also affect adults. During
amphibian is 116/m2 for the spring-dwelling salamander unusually severe winters, shallow ponds may freeze to
Eurycea nana, which reaches these densities in mats of the bottom and result in the deaths of anurans hibernat-
algae that serve as shelter and contain an abundance of ing there, as noted for Rana pipiens by Manion and Cory
food (Tupa and W. Davis, 1976). (1952). Also, floods can be devastating to adults. We
found only two individuáis of the small bufonid Atelopus
mindoensis along a 200-m stretch of a mountain stream
FACTORS REGULATING POPULATIONS in Ecuador after a flash flood had scoured away nearíy
Although much has been leamed since F. Tumer's (1962) all streamside vegetaüon. Before the flood we had ob-
review of anuran demography, some of his same basic served 77 individuáis along the same stretch of stream.
questíons need to be addressed more specifically in the A 28-day drought resulted in 99% mortality in a popu-
field and laboratory. What are the causes of age-specific lation of Plethodon shenandoah on talus slopes in Vir-
mortality? How are growth rates and reproductive suc- ginia, but had no perceptible effect on the population oí
cess reflected in population densities and structures? Are P. cinéreas living in adjacent habitats with deep soils
particular populations regulated by density-dependent (R. Jaeger, 1980b).
factors or affected by density-independent factors? Different reproductive strategies also are important
Density-independent factors, parücularly climaüc vari- density-independent factors. This is especially evident in
ability, are especially important in the survivorship of am- the different survivorship curves among five species of
phibian larvae. After a 4-year study of a population of Desmognathus; Organ (1961) showed that the series—
Ambystoma tigrinum, Semlitsch (1983) concluded that D. quadramaculatus, montícola, fuscus, ochrophaeus.
environmental factors affecting the drying rate of ponds wrighti— is not only one of progressively greater terres-
were the most important mechanisms controlling larval trialism but also one of progressive increase in survivor-
population size; in some years, no young were recruited ship through the early years of sexual maturity (Table
into the postmetamorphic population, but in a year with 11-5). The variability in survivorship of aquatic eggs and
favorable climaüc conditions, more than 1000 young sur- larvae is much greater than that of adults. Therefore.
vived and left one pond. Shoop (1974) also implied that reproductive strategies that involve the removal of eggs
climatic variation was responsible for yearly fluctuations and/or larvae from water might enhance survivorship. In
in the recruitment of young of A. macu/atum, and desic- an analysis of reproductive strategies of tropical anurans.
cation of ponds is the primary cause for larval mortality Duellman (1978) emphasized that ephemeral ponds were
in Triturus vulgaris (G. Bell and Lawton, 1975). "preferable" to permanent ponds for egg and larval de-
Amphibian larvae developing in temporary ponds seem velopment because of the absence of predatory fishes.
to be far more susceptible to mortality because of drought One way of increasing survivorship in temporary ponds
than are those that develop in permanent bodies of water. is the production of múltiple small clutches; in this way.
However, these larvae, too, may not survive some cli- anurans in humid tropical environments do not put all of
matic perturbations, as evidenced when all Ambystoma their reproductive energy into a single large clutch, which
opacum larvae and nearly all Rana c/amiíans tadpoles may desiccate. Moreover, placement of eggs on vege-
overwintering in a pond in Maryland were killed by the tation above water or in floating or arboreal foam nests
pond freezing during a severe winter (Heyer, 1979a). seems to be an adaptaüon for increasing survivorship of
Exceedingly heavy rains or snow melt can cause flash eggs associated with temporary ponds. Hatching at rel-
floods in streams and thereby elimínate or at least greatly aüvely advanced larval stages and rapid growth to meta-
reduce larval populations, such as noted for populations morphosis minimize the duration of the aquatic stage and
of Ascaphus truei by Metter (1968a). maximize survivorship (see Chapter 2 for more extensive
The net effect of these environmental fluctuations is to discussion).
reduce or eliminate a cohort of offspring and thereby Maximizing growth rates is important not only for larval
reduce the size of the postmetamorphic population and stages but also for postmetamorphic individuáis. Preda-
to modify the age structure of the population. For ex- tion pressure is exceedingly high on recently metamor-
ample, Bannikov (1948) showed that population density phosed young anurans, especially by snakes (Tester and
of Rana temporaria was significantly higher in years fol- Breckenridge, 1964; Arnold and Wassersug, 1978) and
lowing breeding seasons with favorable climates than in even by tabanid fly larvae (Jackman et al., 1983).
those years following droughts. The population of Hyla Larval stages of both salamanders and anurans are
 Population Biology
a-biect to heavy predation in permanent ponds by fishes and leeches. A more complex situation was described for 373
and in temporary ponds by insects, such as diving beetles Pseudacris tríseríata by D. Smith (1983). In temporary
srd dragonfly larvae (see Chapter 10). In temporary ponds pools on the rocky shore of Isle Royale, Michigan, pools
T. the American tropics, tadpoles also are eaten by the near the lake shore frequently do not persist for the dura-
smivorous tadpoles of Ceratophrys and Leptodacíy/us tion of the larval period. In other pools, predation by
sntadacty/us (Heyer et al., 1975). Natural mortality dragonfly nymphs (Anox) eliminates most or all tadpoles.
srtong larvae of Ambystoma tigrinum was caused mainly In other pools that persist and lack Anax, competition
by predatíon (J. Anderson et al., 1971). Calef (1973) exists for food, and survivorship of tadpoles is density-
sributed most of the mortality of tadpoles of fíana au- dependent. In some aquatic sites, especially temporary
«ora in Britísh Columbia to predation, because (1) tad- ones, density-independent factors, such as unfavorable
poles kept in the laboratory on starvaüon diets survived climatic conditions, can be most important in determining
rx many weeks, even though they did not grow; (2) survivorship, whereas in these same sites during periods
sopóles living in densities up to 100 ümes normal could of favorable climatic conditions and in permanent ponds,
5-zvive and grow to metamorphosis in the absence of resource availability and competition can be major con-
rredators; and (3) predation rates observed in the field trolling factors. The importance of predation can be ne-
snd simulated in the laboratory were sufficient to account gated by adverse environmental conditions, and the im-
far much of the mortality observed in the natural popu- portance of competition may be negated by intense
len. predation.
However, other studies have concluded that density- Although the interactions of these factors are complex,
dependent intraspeciflc competition is the factor control- an understanding of the regulation of larval populations
irg survivorship of larvae. Thus, on the basis of field and is emerging. However, the mechanisms controlling the
aboratory experiments, survivorship is negatively den- populations of adults are not so well understood. It is
sty-dependent in Ambystoma maculatum (Wilbur, 1972), assumed that most adult amphibians are lost to the pop-
Bu/o americanus (Wilbur, 1977b), Rana íigerina (Dash ulation through predation or disease, but adequate docu-
3nd Hota, 1980), and Scaphiopus holbrooki (Semlitsch mentation is lacking. Catastrophic, density-independent
and Caldwell, 1982). Not all species respond in the same events (e.g., effects of drought onPlethodon shenandoah
*By to increased densities. Comparable field experiments and floods on Atelopus mindoensis) are unpredictable
jn three species of Ambystoma in Michigan by Wilbur and can cause crashes of local populations.
1972) showed that A. laterale increased both the num- Few studies document density-dependent effects on
ber of survivors and the percentage survivorship when populations of adult amphibians. Tyler (1976) reported
ríe density of conspecifics was increased, presumably by that a population of Bufo marinus in New Britain had
irrviding available food among smaller larvae and by in- increased to the point that available insects became scarce
rreasing the larval period. An increase in density of and emaciated toads died daily. The increase in numbers
A tremblayi resulted in a higher number of survivors of Eleutherodactylus coqui in study plots provided with
without a higher percentage of survivorship, but the lar- bambeo retreats, which are defended and used as ovi-
vae were smaller and required a longer time to reach position sites (Stewart and Pough, 1983), suggests that
—etamorphosis. At high densities, only a few larvae of shelter and oviposition sites may be a limited resource
A maculatum survived, but these were large and grew and therefore a density-dependent factor regulating pop-
rapidly. Wilbur concluded that the effect of larval density ulations of that frog. Although predation probably is the
DO A. maculatum occurred early in their development major mortality factor in adults of Hyla rosenbergi, Kluge
and that the few larvae which survived this competition (1981) suggested that injuries resulting from male-male
•A-ere able to exploit the food supply and grow rapidly; combat in the defense of nests might be an important
on the other hand, the plástic growth rates and variable factor in regulating the number of males.
sizes at metamorphosis of A. laterale and A. tremblayi The accumulating data on the dispersión of juveniles,
are adaptations to the uncertain environment of tempo- fidelity to breeding ponds, limited home ranges of non-
rary ponds. aggregative breeders, and shapes of home ranges sug-
Factors regulating survivorship of amphibian larvae may gests that populations are made up of demes that have
change temporally and spatially, even in adjacent ponds, individual characteristics of growth, survivorship, and
as demonstrated for Bu/o americanus by Brockelman structure. This phenomenon has been documented best
1969). In one of his experimental ponds, time of meta- in Notophthalmus virídescens (Gilí, 1978). These popu-
morphosis, individual growth variability, and mortality were lational or demic parameters have genetic implications.
related directly to initial tadpole density, and size at meta- Inger et al. (1974) found that genetic homogeneity was
morphosis was related inversely to initial tadpole density. negatively correlated with the degree of movement for
In a second experimental pond, there was a lack of sig- breeding purposes (see Chapter 16). Samallow (1980)
nificant density effects; high mortality rates were affected noted distinct temporal changes in alíele and/or genotype
by an abundance of predators, chiefly dragonfly nymphs frequency distributions within cohorts of young Bufo bo-
ECOLOGY
274 reas and concluded that mortality among young toads population dynamics of amphibians, it is essential that
was not genetícally random. Thcse studies emphasize the invesügators standardizo the parameters and their
necessity of integratíng ecological and genetic studies of measurements. The usefulness of many of the existing
natural populations. data is extremely limited because comparisons cannot be
If real progress is to be made in understanding the made, and a meaningful synthesis is impossible.
 CHAPTER 13
Toñilly understand an assemblage or a
zmmunity, not only musí its structure be
C-JCMTI but theflow ofenergy and materials
mnong species musí be assessed. Both
«ese aspeas are i'n their infancy as far as
ktrpetofaunal assemblages are concerned.
onimimity
Harold Heatwole (1982)
cology and
pecies

C 'oexisting species of organisms consütute a com-

munity or assemblage, within which interacüons may oc-
tisücal validity of much of the indirect evidence that has
been cited in support of the role of competition in struc-
oir among species. Basically this chapter addresses the turing communities. Strong et al. (1979) and Simberloff
=n\icture of amphibian communities and examines the (1983) suggested that much of the purported structural
patterns of assemblages in different parts of the world. pattern in vertébrate communities simply reflects inter-
Adequate studies of amphibian communities are piüfully specific variation in ecológica! attributes usually associ-
íew, and only in a few cases have the mechanisms regu- ated with resource utilization, rather than a systemaüc
lating community structure been demonstrated. parütioning of resources consisten! with competition and
niche theory.
Studies of amphibian communities have been uneven
COMMUNITY STRUCTURE in their approaches and thoroughness. Most studies of
Until recently, theoretical community ecology has been salamanders have emphasized the ecological relation-
dominated by the assumption that interspecific compe- ships of two or just a few sympatric or parapatric species,
ntion is of primary importance in the determination of whereas many anuran communities have been studied
species composition in most communities (Roughgarden, in their totality but in less detail. Nothing is known about
1983; Schoener, 1983). Most inferences about interspe- caecilian communities.
cific competition concern exploitative competítion—use It is necessary to distinguish between experimental and
of the same resource by two or more species of organ- observational studies of amphibian communities. In ex-
isms—but some studies have demonstrated interference perimental studies (e.g., Inger and Greenberg, 1966;
competition—one organism limiüng another species' ac- Hairston, 1981; Morin, 1983a) the numbers of one or
cess to a resource. However, predaüon may affect dif- more species are directly altered, and changes in the
ferentially the relative abundance of coexisting species abundance or behavior of other species are monitored.
and thereby have a profound effect on the outcome of Such experiments can demónstrate unequivocally the
interspecific competition; also predation may affect the existence of interspecific interactions. However, without
species compositíon of communities. Recent reevalua- a detailed knowledge of natural history, the mechanistic
tions of earlier descriptive studies of vertébrate commu- basis of the interaction may be obscure (e.g., Hairston,
nities (e.g., Strong et al., 1979) have questíoned the sta- 1981), thereby making it difficult to assess the generality
275
ECOLOGY
*'6 of the experimental resulte. Moreover, for obvious logis- or P. glutinosus (warmer and drier). However, in the
tical reasons, experimental manipulations usually involve Balsam Mountains the two species are more broadly
only a féw species, may extend through only a fraction sympatric, apparently because of less intense interspecific
of a generation, and may be conducted at spatíal scales competition.
inappropriate for understanding community dynamics. Salamanders of the genus Desmognathus occur in a
Most observaüonal studies emphasize resource parti- variety of sympatric assemblages and display interesting
tioning—the differential uülizaüon of the physical and/or patterns of microhabitat partitioning. In the southern Ap-
biotic environment by different species. Commonly this palachian Mountains, three to five species form an array
has been accomplished by measurements of a resource from aquatic to terrestrial habítate. Both moisture and
matrix (niche breadth) of a species and of the associatíon predaüon gradiente exist along this habitat gradient. Al-
of two or more species with respect to one or more re- though Hairston originally interpreted the microhabitat
sources (niche overlap) (see Hurlbert, 1978, for discus- partitioning of these salamanders as the result of inter-
sion and formulas). These measurements form the bases specific competition, he (1980) hypothesized that pre-
for the determinaüon of the community structure. daüon is the primary factor structuring salamander niches
Because of the different approaches used in their re- along the gradient. Alternatívely, differences in habitat
spective studies, communities of terrestrial salamanders, and food size resulüng in differences in body size may be
terrestrial anurans, and aquatic larvae are discussed sep- interpreted as the resulte of interspecific competition. Evi-
arately. Much of the material has been taken from Toft's dence for the occurrence of interspecific competition in-
(1985) review of resource partitioning in amphibians. The cludes niche shifts between allopatry and sympatry among
study of amphibian communities is difficult because of three species of Desmognathus in Pennsylvania (Krzysik,
potentíal interactions at different stages in the life cycle. 1979) and in two species in Florida (Means, 1975). Pre-
Furthermore, it should be kept in mind that much of the sumably different factors—competition, predation, and
structure of amphibian communities may result from in- physiological tolerances—vary in importance in different
teractions between amphibians and other organisms (e.g., communities.
bat predaüon on anurans; Tuttle and M. Ryan, 1981)
rather than from interspecific interactions among am- Anurans
phibians alone. Studies of anuran communities have analyzed habitat-
specific assemblages—forest-floor, stream-edge, and
Terrestrial Salamanders breeding-pond communities— as well as entire tropical
Plethodontíd salamanders have been the subjects of many communities.
ecological studies. Hairston's (1949) pioneering work on
several species of Plethodon in the Applachian Moun- Forest-Floor Communities. Assemblages of anu-
tains documented elevational and macrohabitat differ- rans living amidst leaf litter on the forest floor are much
ences and food-size partitioning; the patterns were inter- like trióse of salamanders in that the same species inhábil
preted as the result of interspecific competition. Subsequent the área throughout the season of activity. The numbers
intensive studies on pairs of species of Plethodon were of species and densities of anurans inhabiting the leaf
performed by various workers—Dumas (1956) on P. dunni litter in tropical foreste have been summarized by N. Scott
and vehiculum, R. Jaeger (1971, and papers cited therein) (1982), who noted that the numbers of litter-inhabiting
on P. cinereus and shenandoah, and Hairston (1983b, anurans are much higher in the American tropics than in
and papers cited therein) on P. glutinosas and jordani. África, Borneo, or the Philippines, but diversities are sim-
Fíela experiments showed that closely related species of ilar in wet foreste of Costa Rica and Borneo (Table
Plethodon can compete strongly under natural condi- 12-1).
tions. Sharp habitat partitioning—narrow elevational Toft's (1982 and citations therein) work on anurans
sympatry in P. jordani and glutinosas and microhabitat living in the litter in tropical foreste in Gabon, Panamá,
parapatry in P. cinereus and shenandoah— resulte from and Perú showed that resources are partitioned in dif-
this intense competition. These are examples of interfer- ferent ways depending on the species and on environ-
ence competition for space under logs on the forest floor. mental conditions. For example, litter-inhabiting anurans
Plethodon are territorial, and in defense of their territories have specific local distributions along moisture gradients
they may inflict wounds on intruders. In the case of between ridges and ravines in Panamá, but in homoge-
P. cinereus and shenandoah, the former is more aggres- neous locations in Perú and Gabon, anurans do not par-
sive and is expanding its range, whereas P. shenandoah, tition the microhabitat. Seasonal and diel activities are
which can tolérate drier conditions than P. cinereus, is partitioned in all tropical forest habítate; in the American
becoming restricted to dry talus slopes that are uninha- tropics this is especially evident in comparing diurnal den-
bitable by P. cinereus. In the Smoky Mountains, P. jor- drobatids with the mostly nocturnal Eleutherodactylus
dani and glutinosus have only slight elevational sympatry (Duellman, 1978; Toft and Duellman, 1979).
in a narrow zone where fluctuating environmental con- Among tropical litter inhabitants, food is partitioned by
ditíons alternately favor P. jordani (cooler and moister) both prey size and type. As emphasized by Toft (1985 .
 Community Ecology and Species Diversity
Table 12-1. Comparaüve Numbers of Species of Anurans Inhabiüng the Leaf Litter in Lowland Tropical Forests 277
RainfaH (mm) Number of
Locality Latitud» [dry months] species Reference
Umbé, Cameroon 4°N ±4000 [3] 12 N. Scott (1982)
Hakokou, Gabon 1°N ± 1700 [?] 4* Toft (1982)
Sekaerat, Thailand 14°N ± 1500 [6] 8 Inger and Colwell (1977)
Negros Island, Philippines 9°N 1430 [4] 11 W. Brown and Alcalá (1964)
Ñenga Tekalit, Borneo 1°N 5000 [0] 19 Lloydetal. (1968)
Guanacaste, Costa Rica 10°N 1670 [6] 7 N. Scott (1976)
12 Selva, Costa Rica 10°N ±3600 [1] 20 N. Scott (1976)
Sr.cón de Osa, Costa Rica 9°N ±4000 [2] 19 N. Scott (1976)
Skigandi, Panamá 9°N 2000 [3] 19 Heatwole and Sexton (1966)
Barro Colorado island, Panamá 9°N 2700 [4] 12 Myers and Rand (1969)
ffio Canción, Panamá 8°N 2000 [5] 9 Heatwole and Sexton (1966)
Santa Cecilia, Ecuador 0°N 4400 [0] 30 Duellman (1978)
Beiém, Brazil 2°S 2860 [6] 9 Crump (1971)
fio Uullapichis, Perú 10°S 2220 [2] 25 Toft and Duellman (1979)
*Dry season only.

fcere are two adaptíve peaks of foraging modes—sit-and- tition may be more important and that the species has
•ait foragers and widely ránging, searching foragers. These broader physiological tolerances than recognized previ-
peaks are not exclusive, for some species are interme- ously (Toft, 1985). Pough et al. (1977) observed a similar
iate in their foraging strategies. Moreover, differences in physiological basis for habitat partitioning among Jamai-
physiological, morphological, and behavioral attributes can Eleutherodactylus.
sásl among species using these adaptive strategies. Sit-
2r.d-wait foragers usually are cryptically colored and are Stream-side Communities. Some species of anu-
rapable of activity bursts to capture a few large prey or rans are restricted to riparian habitáis and other species
n escape predation. Active foragers concéntrate on small, move to streams for breeding. Three streams in Sarawak
:ommon prey and are capable of sustained, low levéis in northern Borneo supported 24 species of anurans (In-
oí activity (A. Bennett and P. Licht, 1973; Taigen and ger, 1969). The nine most abundant species were grouped
Pough, 1983). Also, many active foragers are highly toxic into four ecological types: (1) four large species that are
=r.d aposematically colored. Because of the coevolution strictly terrestrial, riparian, and weakly clustered in their
of physiological, morphological, and behavioral traits distribuüons; (2) two small to large species that are par-
jeading to these adaptive peaks, these differences would tially arboreal, riparian, and weakly clustered; (3) two
sxist in the absence of interspecific competition. How- small to large species that are partially arboreal, riparian,
ever, interspecific competition seems to be evident within and strongly clustered; and (4) one large, mainly arbo-
jeeding guilds of these anurans. For example, patterns of real, strongly clustered species that is not restricted to
bod-size partitioning among the ant-eatíng guild in ho- stream banks. Populations of Rana blythi, ibanorum, and
mogeneous forests in Perú show that there is consider- macrodon were manipulated by the removal of one spe-
able overlap in food, but this overlap diminishes during cies from one stream and of a second species from an-
ríe season of lower food abundance (Toft, 1980a). The other stream. The removal of a species resulted in an
same is true for species of Eleutherodactylus in the non- increase in numbers of individuáis of the other two spe-
ant-eaüng guild in Panamá (Toft, 1980b). Similar trophic cies; thus, Inger and Greenberg (1966) concluded that
partitioning exists among four species of West Indian interspecific competition affected population size.
Eteutherodacfylus (K. Jones, 1982). Syntopic species pairs
¿ffer in the size of the prey eaten; three species are sit- Breeding Ponds. Many species of anurans migrate to
and-wait foragers on foliage and one is an active diurnal temporary ponds for breeding; during the time that they
forager. are at the ponds the potential exists for interspecific in-
Although competition may play a role in microhabitat teractions. Because of different species-specific tolerances
partitioning in litter anurans, specific physiological toler- to temperature and responses to rainfall, different species
ances also are involved (and may be more important). enter the breeding community at different times. This
For example, those species most resistant to desiccation, succession provides a temporal partitioning of the pond
such as the bufonids Ate/opus and Bu/o, inhábil drier (Wiest, 1982, and references therein; Fig. 12-1). More-
ridges in Panamá, whereas those species that are least over, a diel pattern is evident among some species. In a
resistant— Co/osíethus, small Eleutherodactylus, and temporary pond in Kenya, six species were most abun-
Dendrobates auratus— are in ravines. However, on Ta- dant in the pond early in the evening and four were most
boga Island, D. auratus has no anuran competitors and abundant in the middle of the night (R. Bowker and M.
forages in dry áreas; this suggests that perhaps compe- Bowker, 1979).
ECOLOGY
378
^30-

Figure 12-1. Anuran succcssion in a temporary

pond in Brazos County, Texas. A. Monthly
rainfall (October 1972-September 1973) in
centimeters. B. Mean monthly máximum and
mínimum temperatures (°C). C. Anuran
succession. Solid bars = calling males; shaded
bars = breeding; open bars = larvae.
Abbreviations for species: Ac = Acrís crepitan»,
Bs = Bu/o speciosus, Bv = B. valliceps, Go =
Gastrophryne olivácea, Hv = Hyla versicolor,
Pe = Pseudacrís clarki, Ps = P. streckeri, Pt =
P. tríseríata, Rs = Rana sphenocephala, Sh = O N D J F M A M J J A S
Scaphiopus holbrooki. Based on Wiest (1982).

Among tropical anuran breeding assemblages, vocali- that the pattern of acoustic parüüoning is similar in dis-
zation was deemed to be the primary factor separaüng junct communities of like habitat but with different spe-
species, followed by calling sites and oviposition sites, for cies compositions.
10 species of hylids in Costa Rica (Duellman, 1967b) Resource partitioning among synchronously breeding
and for 5 species of hylids in Brazil (Cardoso, 1981). species also involves calling sites and oviposition sites,
Results of analyses of calis of hylid frogs in breeding com- but the most importan! factor seems to be advertisemen:
munitíes in Costa Rica, Brazil, and Ecuador led Duellman calis (see Chapter 4). As examples, Creusere and Whit-
and Pyles (1983) to suggest that the acoustic environ- ford (1976) concluded that among five synchronousty
ment is partitioned in particular anuran communiües and breeding species of anurans in the Chihuahuan Desert ir.
 Community Ecology and Species Diversity
\e*p México, advertisement cali was the primary ecolog- from the ground to bushes and to trees. All bush- and 279
jc¿ factor allowing for species recognition, and the sec- tree-dwelling species are nocturnal. The terrestrial sub-
:rc factor was calling site. R. Humphries (1981) noted community in the forest consists of species that are as-
ta: the presence or absence of other species did not sociated with swamps and those in the leaf litter; this
jcsct the tíming, intensity, or duration of breeding activity subcommunity is further divided into nocturnal and diur-
D. a given species in a breeding community of 11 species nal species.
ai anurans using a pond in Australia. He hypothesized Although 81 species occur at Santa Cecilia, differences
ta: distinct advertisement calis are important in resource in activity cycles, microhabitat preferences, and feeding
perátíoning by anurans. habits result in numerous guilds that have little or no
overlap. Furthermore, these anurans have diverse repro-
Tropical Communities. Because of their abundance ductive modes, so they are using different oviposiüon
xxi diversity in the wet tropics, anurans have been the sites, and their tadpoles (if present in the mode of life
5_bjects of several community studies. The most com- history) develop in diverse aquaüc habitats (Fig. 12-2).
rrehensive of these is Duellman's (1978) analysis of the Duellman (1978) concluded that this large number of
-erpetofauna at Santa Cecilia on the Equator in Ama- species could coexist because of the absence of, or little
zxúan Ecuador, where temperature and photoperiod are pressure from, interspecific competition and that the ab-
jeatively stable throughout the year and rainfall is more sence of interspecific competition was the result of: (1)
or less evenly and abundantly distributed throughout the the abundance of available resources; (2) structural het-
year. Eighty-one species of anurans occur at Santa Ce- erogeneity of the environment; (3) climatic equability of
de. These were analyzed with respect to macrohabitat the environment; and (4) differential spatial and temporal
•primary forest, secondary forest, clearings), microhabitat utilizaüon of resources by the fauna. Furthermore, he
srrestrial, bush, tree), diel activity (nocturnal, diurnal), suggested that populations were controlled by unpre-
sr.c food. dictable environmental fluctuaüons and by predaüon, so
Eleven of the 69 species in the primary forest are re- abundances are kept in check below the level where
sricted to that habitat; 58 of these are among the 68 competition might be important.
5-»cies occurring in the secondary forest (3 restricted there). Similar patterns of resource uülization were docu-
Bghteen of the specie? in the primary forest and 25 in mented for 53 species of anurans in a seasonally dry
±ae secondary forest are among the 26 species occurring rainforest in Amazonian Perú (Toft and Duellman, 1979)
r. clearings (1 restricted there). Therefore, 18 species are and for 37 species at Belém, Brazil (Crump, 1971). A
—acrohabitat generalists and 15 are macrohabitat spe- comparison of anuran communities in adjacent áreas of
zalists. In the primary forest, 24 species occur in trees broadleaf evergreen forest, deciduous dipterocarp forest,
rr.ore than 1.5 m above ground), 46 in bushes, and 39 and agricultural land in northeastern Thailand (Inger and
or the ground or amidst leaf litter (some species occur Colwell, 1977) revealed that in that seasonally dry región
in more than one microhabitat). The same categories in only 24 species of anurans occurred. Nineteen species
~c secondary forest have 20, 48, and 31 species, and were found in the evergreen forest, 20 in the deciduous
in the clearings O, 14, and 16 species. The only diurnal forest, and 19 in the agricultural land, with the greatest
Togs are on the forest floor; 7 species there are entirely faunal overlap between the evergreen and deciduous for-
¿urna!, 9 are both diurnal and nocturnal, and 13 are ests. Larger and more distinct guilds existed in the ev-
rompletely nocturnal. ergreen forest (most predictable habitat) than in the other
Four major feeding guilds were recognized. Actively habitats. Inger and Colwell (1977) suggested that unpre-
üoraging terrestrial species that specialize on ants include dictable environments tend to prevent the formation of
íve dendrobaüds, four bufonids, and five microhylids; in distinct guilds, which are an expression of specialization
addition, one Eleutherodactylus and two hylids (Sphae- in resource use; therefore the greater species richness of
-.orfiynchus) specialize on ants. The terrestrial leptodac- more predictable habitats may be a function of guild for-
lyüd Physalaemus petersi eats only termites. Two species mation.
are carnivores and feed on frogs—the terrestrial Cera-
-jjphrys comuta and the arboreal Hemiphractus probos- Aquatic Larvae
ddeus. The other species of anurans in this community Most studies of larval communities have been concerned
are sit-and-wait foragers and eat a variety of prey, of with anuran tadpoles, but the effects of salamander lar-
A'hich orthopterans are the most abundant Ítems, fol- vae of some salamanders, principally Ambystoma and
Jowed by coleopterans, lepidopterans, and homopterans. Notophthalmus, on tadpoles also have been investigated
In this community, the macrohabitat is only weakly (e.g., Wilbur, 1972; Morin, 1981). Amphibian larvae lend
partitíoned; the secondary forest contains a slightly de- themselves to field and laboratory manipulations, and
paupérate assemblage of the primary forest. The sub- numerous experimental studies have provided an un-
community in clearings primarily is made up of a few derstanding of the mechanisms of community structure
species that also occur in the forests. By contrast, within in these organisms. However, the resulting interpretations
the forest there is striking vertical stratification of species are not always consistent. For example, an Ambystoma-
ECOLOGY
280

Figure 12-2. Community structure

of 69 species of anurans inhabiting
primary lowland rainforest at Santa
Cecilia, Ecuador. Each cell in the
grid represents a combination of
microhabitat and site of egg
development. Gíreles are sit-and-wait
foragers; squares are active foragers
feeding primarily on ants. Solid
symbols are nocturnal species; open
symbols are diurnal species; open
symbols with dark centers are
diurnal and nocturnal species.
Lengths of lines leading to the
symbols represent the numbers of
individuáis collected. Symbols noted 0#
a, b, and c indícate three species that
are active in one habitat by day and ^
another by night. Based on data in
Duellman (1978).
^

Rana community in Michigan was considered to be struc- G/yphog/ossus molossus and Po/ypedates íeucomystax
tured primarily by interspecific competítion (Wilbur, 1972), contributed most heavily to the biomass, but the peak o:
but the structure of tadpole communities in Maryland, the former was in April and of the latter in June.
Panamá, and Thailand were considered to be the result Anuran larvae are highly specialized "feeding ma-
of adaptive modifications of the tadpoles, environmental chines." Tadpoles have distinct interspecific differences
fluctuations, and predaüon (Heyer, 1976, and references in mouth structures and thus differ in their abilitíes to
therein). gather food in different macro- and microhabitats. More-
Amphibian larvae, especially tadpoles, exploit the ex- over, structural differences are related to their abiliües te
traordinarily rich, but sometimes highly transient, aquatic inhabit flowing or still water, as well as their positions ir.
environments that are at least seasonally available. Anu- the water column (see Chapter 6). Macro- and micro-
ran larvae have been shown to partitíon resources in habitat partitioning is primarily a result of the adaptive
these temporally fluctuating environments. This partition- modifications of the tadpoles. For example, in a strearr.
ing is evident with respect to macro- and microhabitat community in Panamá, the tadpoles of Colostethus nu-
within a temporal framework. Temporal partitioning is bicola have an anterodorsal mouth and feed on the sur-
conspicuous within tadpole communities, as shown for face; tadpoles of Centrolenella fleischmanni have ventral
températe forest ponds by Heyer (1976), Seale (1980), mouths and long, muscular tails and feed amidst the de-
and Wiest (1982), for tropical ponds by Dixon and Heyer tritus on the bottom, and tadpoles of Smilisca si/a have
(1968) and Heyer (1973), and for a tropical stream by anteroventral mouths and weak tails and feed on the
Heyer (1976) (see Fig. 12-1). For example, among 10 bottom of quiet pools (Heyer, 1976). The tadpoles of
species of anuran larvae developing in each of two ponds Colostethus are present throughout the year, Centrole-
in Thailand, no more than 5 were found at the same time nella in the rainy season, and Smilisca in the dry season
in one pond and 6 in the other (Heyer, 1973). Further- when water flow is minimal.
more, densities of synchronously developing tadpoles Macrohabitat partítioning in the choice of types of ponds
showed temporal differences; at one pond, tadpoles of or streams is a matter of choice by the adults; survival o:
 Community Ecology and Species Diversity
te iarvae is dependent on their hatching (or being placed) occur under natural conditions (Seale, 1980). Density- 281
r 2 suitable aquatic habitat. Heyer et al. (1975) argued dependent interspecific competition for food has been
-üfíctively that predation influences tadpole survival and demonstrated primarily in experimental conditions (Morin,
zrval community structure in ponds in the tropics; be- 1983b, and references therein).
2i_se ot differing risks of predation, similar kinds of hab- Exploitative competition for food is the ultímate threat
JSEL partítioning occur in températe ponds (Heusser, 1970a; at high densities, but the proximate competitive factor is
Woodward, 1982b). Avoidance or reduction of predation interference, which is mediated by growth inhibition, both
is accomplished by larvae inhabiting ephemeral ponds, intra- and interspecifically (see Chapter 6). By inhibiting
«ere aquatic predators are few or absent. Larvae that the growth of another species, the superior competítor
arabit permanent aquatic environments also inhabited decreases its own time to metamorphosis while increasing
•y. aquatic predators have mechanisms to avoid preda- that of the inferior competitor. Because of differential rates
icr. For example, in Panamá, tadpoles of Bufo typhon- of predation on different sizes of larvae and at difieren!
as have noxious skin secreüons and survive in large pools times during the season, the outcome of interspecific
ir streams inhabited by the predatory tadpoles of Lep- competition can be altered by such inhibition (Morin,
rrócty/us pentadactylus (Wells, 1979). Tadpoles oíHyla 1981).
seyjraphica move about in large schools in lakes inhab- It is evident that the structure and maintenance of lar-
ÍEC by many species of predatory fish (Duellman, 1978); val communities are dependent on complex iníerrelation-
xrooling presumably reduces predation. ships of physical factors, predation, and intra- and inter-
Microhabitat partitioning by larvae that develop syn- specific competition. Furthermore, the effecls of these
rronously is accomplished principally by the positioning factors change with respecí ío temporal utilization of the
of iie larvae in the water column, as noted for tadpoles environment by different species with respect to the dura-
by Heyer (1973) and Ambystoma larvae by J. Anderson tíon of development.
irc Graham (1967). Presumably, partitioning of food by
sfpoles is a funution of, first, the abilities of various spe-
oes to ingest particles of difieren! sizes and, second, the SPECIES DIVERSITY
rcsnon of the tadpole in the water column (Heyer, 1974c). The concept of species diversity as a unitary measure
^ir-.ough exploitative interspecific competition for food involving both the numbers of species (richness) and rel-
anong tadpoles has not been demonstrated convinc- ative numbers of individuáis per species (equitability) has
ñgiy. the diversity of foraging behavior and buccal struc- received considerable attention (see Pianka, 1977, for
«res for ingesting particles of food of specific sizes sug- review). Species richness is simply the number of species,
:es3 that food is partítioned, and that the more generalized whereas equitability indícales how individuáis in a com-
JK ders may be able to overlap with several other species. munity are distributed among species. If all species in a
On the other hand, the tadpoles of Gastrotheca com- community contain the same number of individuáis, the
aaonly are the only tadpoles in ponds at high elevations apportionment is maximally equitable. If some species
r ihe Andes; these tadpoles have extremely generalized are abundant and some rare, the distribution is inequit-
buccal structures that allow them to ingest a wide spec- able. Several ecologists (e.g., Peet, 1975) have argued
r_m of particle sizes (Wassersug and Duellman, 1984). that the concept of species diversity is biologically mean-
The factors regulating larval communities in temporary ingless, because it encompasses two sepárate concepts
ponds are correlated with the duratíon of larval devel- (species richness and equitability). Therefore, these com-
opment. Environmental uncertainty and predation put ponents of species diversity of amphibians are discussed
icsolute limits on the máximum time that larvae can re- separately.
—¿in in the pond before metamorphosing (Wilbur and
Collins, 1973). The probability of the pond drying up Species Richness
«creases with the time of residency in the pond. Also, Generally it is known that the number of species of ec-
•he longer a pond is in existence, the greater will be the tothermic vertebrales is higher in the tropics than at high
accumulation of predators and the risk of predation. In- latitudes. Although this is not necessarily true of sala-
vasión of small ponds by predators may result in the manders, it is true of anurans (Table 12-2). General, broad
•Exnncüon of all larvae in the pond (Morin, 1983a; patterns of species richness in amphibians as a group
D Smith, 1983). Both intra- and interspecific competition show latitudinal trends, such as an increase from 10 to
s correlated with relative limits of time in temporary ponds. 40 species between Maine and Florida in eastern United
ir. the absence of predation, or even in the presence of States (Fig. 12-3). However, integrated with the latitu-
predation (Woodward, 1982c), population sizes of larvae dinal trend are trends along moisture gradients. For ex-
:an increase to the point of intense competition. Field ample, in North America, the greatest numbers of species
soidies have documented that tadpoles can have an ex- are in áreas of high rainfall, principally in southeastern
reme impact on food density (principally algae) in nat- United States and secondarily in the northwest.
ural ponds, and suggest that competition for food can Comparisons of amphibian species richness among
ECOLOGY
282 Table 12-2. Latitudinal Gradient in Anuran Species Diversity in the New World
Dcgrees N. Number of
Site latitude species Reference
Georgc Reserve, Michigan 42 8 Collins (1975)
University of Kansas Reservation 39 9 Fitch (1965)
Brazos County, Texas 31 11 Wiest (1982)
Tehuantepec, México 16 17 Duellman (1960)
Barro Colorado island, Panamá 9 19 Myers and Rand (1969)
Santa Cecilia, Ecuador 0 81 Duellman (1978)

Figure 12-3. Species densities of amphibians in

North America constructed from compilation of
numbers of species in grids of 100 miles square
(160 kilometers square). Note the mercase in
number of species to the southeast and less so
to the northwest, both áreas characterized by
high rainfall. A península effect (diminishing
number of species) is evident in peninsular
Florida. Redrawn from Kiester (1971).

various regions in the tropics emphasize the importance positively associated with the amount of rainfall anc
of moisture to the richness of the amphibian fauna. For negatively associated with the number of dry months
example, a strong gradient in the number of species from (Table 12-1).
south (high number) to north (low number) in the Yu- Among anurans, generally there is a decrease in the
catán Península is strongly correlated with the amount of number of species with altítude, although local enviror-
rainfall (J. Lee, 1980). A latitudinal gradient correspond- mental conditions may alter this gradient. A transect es-
ing to decreasing moisture is evident in the numbers of sentíally along the Equator from the Amazon Basin te
species of amphibians in supratreeline habitáis in the the eastern crest of the Andes reveáis that at 340 m in
Andes; the moist páramos in Colombia and Ecuador sup- the tropical rainforest as many as 81 species of anurars
port up to five species, whereas only one species is present exist in one community. At elevations of 1400-1600 rr.
in the dry parts of the Altiplano in northern Argentina in cloud forest, the largest community consists of 23 spe-
(Péfaur and Duellman, 1980). Even at the same latitude, cies, and at elevations of 2500-2700 m only 17 species
this moisture gradient is apparent. At Belém, Brazil, at coexist. Richness diminishes to only 5 species in subpar-
the mouth of the Rio Amazonas, rainfall amounts to about amo habitats at elevations of 3000-3200 m and to 4
2800 mm annually but is unevenly distributed, so that species in páramo above 3500 m (Fig. 12-4).
most of the rain falls in one 6-month season; 37 species Salamanders not only require moist conditions like
of anurans are known from the vicinity of Belém (Crump, anurans but also prefer cooler temperatures. Accordingh..
1971). At Santa Cecilia, Ecuador, in the western part of altitudinal gradients in salamanders commonly differ frorr.
the Amazon Basin, about 4400 mm of rain falls through- those of anurans. For example, among 15 species <x
out the year; 81 species of frogs are known from Santa plethodontid salamanders recorded along a transect in
Cecilia (Duellman, 1978). Within anuran communitíes southwestern Guatemala (D. Wake and J. F. Lynch, 1976 .
inhabiting leaf litter in tropical forests, species richness is only 4 species occur in tropical forest below 1000 m. f
 Community Ecology and Species Diversity
occur at elevations of 1000-2000 m, and 10 live be- Altítudinal changes in abundance have been noted for 283
2000 and 3000 m. forest-floor anurans in Costa Rica (N. Scott, 1976); at
two lowland sites the numbers of amphibians on the for-
Abundance and Equitability est floor were 0.12/m2 and 0.15/m2, whereas at 1200 m
rew sufficiently quantitative studies have been carried there were 0.55/mz. A similar increase in abundance was
;ul to pcrmit evaluation of the abundante of amphibians noted among samples of anurans taken at elevations of
r. different regions, although some individual species, 1010, 1200, and 1425 m on the slopes of Cuernos de
ajch as the salamander Plethodon tínereus, have been Negros in the Philippines (W. Brown and Alcalá, 1961).
srudied in detail (see Chapter 11). On the slopes of Volcán San Marcos in Guatemala, the
The only detailed comparisons of amphibian abun- overall abundance of salamanders increases at higher
iance are the works of M. Lloyd et al. (1968) and Inger elevaüons (D. Wake and J. F. Lynch, 1976).
1980a) among communities in tropical forests in south- It has been well documented that in many groups of
eastem Asia and the analyses of forest floor communities organisms, species richness is high in tropical forests, but
TI Central America, África, and southeastern Asia (N. a fallacy that has persisted in the literature is that in trop-
Scott, 1976, 1982; Inger, 1980b). These comparisons ical forests no one species is common, thereby implying
s~.owed that both terrestrial amd arboreal anurans were that equitability is high. As recently as 1976, Maiorana
ar more abundant in diurnal and nocturnal samples from stated, "There are many species in the tropics, but gen-
brests in northern Borneo and peninsular Malaya than erally individuáis of any one of them are rare." This may
T. the seasonally dry forests in northeastern Thailand. For be true for some organisms, such as trees, but consid-
example, the average number of terrestrial, nonriparian erable evidence indicates that this is not true for amphib-
rogs captured per day at Sakaeret, Thailand, was 0. 12 ians. For example, in large samples of anurans inhabiting
in dry evergreen forest and 0.27 in deciduous forest, as the leaf litter in tropical forests in Borneo, the Philippines,
rompared with 1.31 per day at Nanga Tekalit in Borneo. and Central America (reviewed by N. Scott, 1976), the
However, these figures are extremely low in comparison most abundant species was represented by at least twice
-¿Tth those from Central America— 11.6 for Rincón de the number of individuáis of the second-most abundant
Osa, Costa Rica, 14.7 for La Selva, Costa Rica, and 29.8 species, and in some cases the most abundant species
jor Silugandi, Panamá. was represented by more individuáis than all of the other

400°- Páramo

Subparamo

3000-- -1 1-
Cloud Forest

42

11
I
: 2000- 1 21
11
61 3

5 1
I
1000- 3342"
Tropical Rainforest
Figure 12-4. Patterns of altitudinal distribution
27 of anurans along an equatorial transect from the
crest of the Andes (Paso de Guarnan!) to the
22 Amazon Basin (Santa Cecilia) in Ecuador.
Numbers denote the number of species having
43 4 3 2 the altitudinal distribution indicated by the
vertical bars. Based on data in Duellman (1978,
Patterns of Altitudinal Distribution 1979).
ECOLOGY
284 Table 12-3. Equitability of Anurans in Leaf Litter at Different Elevations in Costa Rica*
Elevation Number of Number of Number of Most Second-most
Locality (m) plots species individuáis abundant (%) abundant (%)
La Selva 100 19 15 165 42 19
Rincón de Osa 20 20 24 135 37 18
San Vito 1200 10 8 266 83 6
*Based on N. Scott (1976).

species combined. In an aseasonal tropical rainforest at nities and the differences among communities, especially
Santa Cecilia, Ecuador, 5665 anurans representing 81 between those in the tropics and in the températe regions
species were collected (Duellman, 1978). The 5 most (see Pianka, 1966, for review). These are the: (1) evo-
abundant species represented 22% of the total number lutionary time theory, (2) ecológica! time theory, (3) cli-
of individuáis, whereas the five least abundant species (4 matic stability theory, (4) spatial heterogeneity hypothe-
with one individual each, and 1 with two) represented sis, (5) productivity hypothesis, (6) competition theory.
only 0.1% of the total. These figures are biased in that and (7) predation theory. The following discussion of
sampling was not complete; not all individuáis of com- these concepts emphasizes their applicability to amphib-
mon species were collected. ian communities and assemblages.
Comparable data are available from Lost Lake, South The evolutionary time theory advócales that commu-
Carolina, in the eastern United States (S. Bennett et al, nity diversity increases with the age of the community
1980). Among five species of salamanders sampled over From that premise it has been argued that températe
2 years, Notophthalmus virídescens composed 85% and communities are impoverished because of geologicaüy
Ambystoma opacum only 0.1% of 3641 individuáis. recent glaciations or other disturbances, whereas tropical
Among 11 species of anurans, Gosírophryne caro/inensis communities are older (more mature) and henee more
and Bufo terrestris were the most abundant, composing diverse. However, the idea of the antiquity and immut-
36% and 29%, respectively, of 11,381 individuáis, whereas ability of equatorial rainforests has been challenged ef-
2 species, Hyla squirella and H. versicolor, were each fectively by paleoclimatological and geological evidence
represented by only a single individual. The figures for in support of drastic climatic changes in equatorial regions
temperate-zone anurans are not greatly different from during the Quaternary (see Prance, 1982, for review). In
those for tropical environments. fact, this climatic-ecological fluctuation has been used to
The decline in species richness but increase in abun- explain the richness of the rainforest biotas, including the
dance of individuáis with increasing altitude results in lower diversity of anurans (Duellman, 1982a). Vicariance modeis
equitability at higher elevations. This was demonstrated of three groups of anurans are correlated with the pat-
by N. Scott's (1976) analysis of litter plots at different terns of Quaternary ecológica! changes in the Amazor.
elevations in Costa Rica (Table 12-3), which shows a Basin and provide a historical explanation for the co-
twofold difference in relative abundance of the most existence of closely related species in the upper Amazor.
common species at a montane site as compared with Basin.
lowland sites. This comparison is especially meaningful The concept of ecológica! time deals with shorter time
between one lowland site, Rincón de Osa, and the mon- spans than the theory of evolutionary time and empha-
tane site, San Vito, because the same species, Eleuth- sizes the time required for the dispersa! of species into
erodactylus stejnegerianus (Usted as E. bransfordi by newly opened áreas of suitable habitat rather than the
N. Scott, 1976), is the most abundant anuran at both time necessary for the evolution of new species or for the
sites, but the relative abundance increases from 37% to adaptation of existing species. Ecological time would seerr.
83% from Rincón de Osa to San Vito. The second-most to be an importan! determinan! of diversity only in cases
abundant species (£. /ongirostris— 18%) at Rincón de where there are pronounced barriers to dispersa!. This
Osa does not occur at San Vito, but the second-most idea is most applicable to insular biotas and may explair.
abundant species (E. rídens— 6%) at San Vito composes the absence of some continental species on nearby is-
only 0.7% of the fauna at Rincón de Osa. lands, but in general the theory has little applicability to
The available data indícate that among anuran com- continental amphibian communities.
munities, equitability generally is low in both températe Stability of climate and vegetation créales a stable en-
and tropical communities and that equitability decreases vironment for animáis and allows them to specialize or.
with altitude in tropical regions food and microhabitat. Thus, regions with stable climates
allow the evolution of finer specializations and adapta-
tions than do regions with more erratic climates, because
EVOLUTION OF of the relative constancy of resources. Klopfer and
AMPHIBIAN COMMUNITIES MacArthur (1961) proposed that more species can oc-
Several hypotheses have been proposed to explain the cupy the unit of habitat space, and niches are smalier
numbers of species and individuáis making up commu- (i.e., organisms more specialized) in stable environmens
 Community Ecology and Species Diversity
. -.e mechanism suggested for the control of diversity by uous throughout the year both in montane cloud forest 285
•tse. theory of climatic stability also can apply to climatic and in lowland rainforest, but in the former the leaf litter
jsdictability; thus, a región with a highly predictable but is about twice as deep as in the lowland forests, and the
isrlable annual climatic pattern conceivably could allow montane forests support a greater number of individuáis
apecies to specialize on those resources that are predict- of litter-inhabiting anurans (N. Scott, 1976). The higher
abie from year to year. temperature in the lowlands results in a more rapid rate
b has been shown that many reproductive specializa- of leaf decay, thereby reducing the amount of the micro-
fans in anurans are associated with highly stable envi- habitat.
lonments (see Chapter 2); therefore, the presence of Many plants store the producís of their primary pro-
K:urans having such specialized reproductive modes in duction and expend this stored energy in one great bloom
i given assemblage is dependent on the climatic stability of flowering and seeding; this tends to reduce the stability
or the región. For example, generally the successful de- of the system. In attempting to explain the depaupérate
«dopment of terrestrial or arboreal eggs is dependent on numbers of species and individuáis of amphibians in the
rontinuous high atmospheric humidity; there is a high leaf litter on the forest floor in Indo-Malayan forests as
degree of fidelity of such anurans to regions with high compared with neotropical forests, Inger (1980b) sug-
atmospheric humidity (Duellman, 1982a). The patterns gested that the primary causal factor was the seasonality
oí the complex üming of breeding, gestation, and ovi- of fruiting by the dominant trees. The Bornean and Ma-
position by plethodontid salamanders differs in eastern layan forests are dominated by dipterocarps, trees char-
and western North America and in the highlands of Cen- acterized by the synchronous fruiting of more than 100
kal America; these differences correspond to different but species with intervals between such reproductive explo-
predictable climatic patterns in the three regions (see sions exceeding 1 year. The synchronized fruiting should
Chapter 2). Thus, climatic stability is considered to be a lead to reduction in abundance of an entire group of
major factor in the structuring of amphibian communities arthropod primary consumers during nonfruiting years;
and to be an importan! component of diversity. this should affect the total size of the insect population
Everything else being equal, more complex habitáis and therefore the numbers of insectivorous secondary
should support more species than simpler ones because consumers, such as anurans.
aach species can live on a different part of the environ- The theoretical basis for the role of interspecific com-
mental mosaic. Spatial heterogeneity may exist at several petition in community structure was discussed previously.
levéis. Macrospatial heterogeneity involves topographic However, this concept has been broadened and modified
relief, and it is obvious that topographically diverse re- with respect to latitudinal gradients in species diversity.
gions contain more habitáis (and thus more species) than Dobzhansky (1950) suggested that natural selection is
sopographically simple áreas. This aspect of spatial het- controlled largely by the exigencies of the physical en-
erogeneity is important in between-habitat diversity, and vironment in the températe zones, whereas Ínter- and
the differences in amphibian assemblages in diverse hab- intraspecific competition is more important in determin-
itats were discussed earlier in this chapter. ing the course of evolution in the tropics. Presumably,
Microspatial heterogeneity is significant in explaining natural selection would proceed in a,different direction
within-habitat diversity. Microspatial complexity includes in aseasonal tropical environments because density-inde-
horizontal, vertical, and qualitative heterogeneity of phys- pendent mortality factors such as drought and cold sel-
ical and biotic elements in the environment. Complex dom occur there. According to Dobzhansky's reasoning,
habitáis contain more microhabitats than homogeneous catastrophic mortality usually causes selection for in-
habitats and may contain subcommunities that are absent creased fecundity and/or accelerated development and
in less complex habitats. For example, bromeliads in doud reproduction, rather than selection for competitive abili-
forests in the American tropics provide a microhabitat ties and interactions with other species. These ideas have
that is used by many salamanders and anurans, and some been expanded by various theoreticians to argüe that in
of these species are restricted to that habitat. Therefore, comparison with températe species, tropical species (1)
such species are present only in communities in which are more highly evolved, (2) possess finer adaptations,
that microhabitat is available. (3) have more restricted diets, and (4) have more specific
All other things being equal, regions of greater pro- habitat requirements.
ductivity can support more species than regions of lesser The component arguments of the competition hypoth-
productivity, because each species uses less of the total esis imply that the latitudinal gradient in competition al-
range of resources. Furthermore, a greater number of lows more species to coexist in a given environment;
individuáis can be supported in highly productivo envi- therefore competition for resources is keener and niches
ronments. Productivity is known to be correlated with are smaller. Thus the competition hypothesis makes many
rainfall. Regions of the world having high amounts of of the same predictions as the theory of climatic stability.
rainfall annually support the richest amphibian assem- However, there is one major difference. The competition
blages. However, another component of productivity may hypothesis implies that more individuáis occupy the same
be important for terrestrial amphibians inhabiting the leaf unit of habitat space in more diverse communities, whereas
litter on the forest floor. In Costa Rica, leaf fall is contin- the theory of climatic stability predicts that the same num-
ECOLOGY
286 ber of individuáis will be supported by a unit of habitat, There is no available evidence relating to the first pre-
regardless of the diversity, but there are fewer individuáis diction, but Arnold (1972) demonstrated a latitudinal gra-
of more species in tropical habitats. dient in the number of species of frog-eating snakes cor-
It has been shown that diversity of reproductive modes responding to the gradient in the number of species of
in anurans contributes to increased species richness in frogs. %
humid tropical habitats, but this apparently is in response It is evident from the limited data on amphibian com-
to climatíc stability. Furthermore, it is generally conceded munities that no single factor universally explains the
that spatial heterogeneity provides more microhabitats in structure of these communities. Furthermore, in a given
aseasonal tropical habitats than elsewhere. But does this community the regulating factors may change tempo-
higher number of species in tropical environments mean rally.
that there is more competition? In order to address this Most of the literature dealing with community structure
issue it is necessary to consider (1) the spectrum and and species diversity omits consideration of the history
abundance of available resources, (2) the stability of the of the región and the biota. Each community is an as-
resources, (3) the extent of resource uülizatíon by mem- semblage of species, each one of which has had a sep-
bers of the community, (4) the amount of overlap in árate phylogeneüc history. Although the componen! spe-
resource utilization by members of the community, and cies of an existing community are subjected to the same
(5) the degree to which resources are limiting, rather than environmental variables, prior to the formaüon of this
other factors (e.g., predation). A tenet basic to the entíre community, some of the component species may have
theory of competition is that one or more required re- been subjected to different environmental conditíons and
sources must be limited (demand being greater than sup- may not have been in the same community. Thus, those
ply) for effective competition to occur. There is no evi- species may have evolved prior to coexistence and the
dence that interspecific competition is greater in amphibian evolution of some of the attributes that allow them to
communities in the tropics than in températe habitats. exist in the present community. It is most unlikely that
Advócales of the predation hypothesis suggest that there the component species evolved syntopically and that the
are proporüonately more predators (individuáis and/or various adaptations of each species evolved in response
species) in the tropics and that by limiting various prey to other species in the present community. Actually the
populations to low densitíes, predators reduce the level adaptations, ecological tolerances, and basic resource uti-
of competition among and berween prey species. Pre- lization probably were established at the time and place
sumably this lower level of competition then allows the of origin of the species, which probably was not in the
addition and coexistence of new intermedíate types of present community. Therefore, an understanding of
prey. As noted by Pianka (1966), two predictions may community structure and of the differences among com-
be drawn from the predator hypothesis: (1) Competition munities in different regions necessitates not only a
among prey species will be less in more diverse com- knowledge of the factors regulating the present assem-
munities than in simpler communities. (2) There should blage of species but also a knowledge of the history of
be an increase in the proportíon of predatory individuáis component species.
and/or species as communities become more diverse.
 PART

MORPHOLOGY
 CHAPTER 13
¿Mough man has a long intellectual
yniogeny behind him, each ofus must
jndergo an educational ontogeny ifwe are
u pick up and proceed where others have
iefioff.
Musculo-
Malcolm Jollie (1962)
skeletal System

"ubstantial portions of this book deal with aspects of cluding the hyobranchial apparatus, the axial compo-
me biology of amphibians that could be described and nen!, and finally the appendicular musculoskeletal sys-
analyzed only with the advent of modern technological tem. Because salamanders are, in most respecta, the most
methodology. Among the oldest studies of amphibians generalized morphologically of the three orders, they are
are morphological descriptions of the macro- and micro- discussed first in each subsection. Myological descriptions
structure of selected organs or organ systems. Observa- of salamanders are the most detailed and nearly com-
ron and description are the morphological premises on plete, and in this chapter they serve as the base to which
which interpretations are founded—interpretations that the muscle complexes of caecilians and anurans are com-
might address the phylogenetic history of form, its func- pared. The ways in which the three units are integrated
ional significance, ontogeneüc development, or varia- to produce the distinctive Bauplan of each order are dis-
ion. Although the species (or populations thereof) is the cussed at the end of the chapter.
operational unit of evoluüon, the morphology of a spe-
cies represents its observable interface with the environ-
ment. Thus, knowledge of the structure of an organism SKULL AND HYOBRANCHIUM
is prerequisite to an understanding of its phylogenetic The cranium and hyobranchial apparatus is a complex
relationships, behavior, and relationship with biotic and and diverse architectural unit in amphibians. As in all
abiotic aspects of the environment. vertebrales, it is the seat of the central nervous system
Although various details of amphibian morphology are and the primary sense organs of sight, olfaction, hearing,
described throughout this book in order to elucídate par- and equilibrium. In anurans laryngeal cartílages derived
ticular subjects (e.g., vocalization, feeding, and so on), from the larval hyobranchial apparatus allow for vocali-
two chapters have been allocated to the treatment of zation. The hyobranchial apparatus lying in the floor of
general structural patterns. The present chapter is dedi- the mouth between the pectoral girdle (anurans and sal-
cated to basic architecture—that is, the musculoskeletal amanders) and the mandible is the foundation for the
system that constitutes the framework of support for the attachment of mandibular, branchial, and tongue mus-
various organ systems described in the following chapter. cles; this musculoskeletal unit is the mechanical system
The musculoskeletal system of adult amphibians can for ventilation as well as securing, manipulating, and in-
be divided into three convenient units—the cranium in- gesting food.

289
MORPHOLOGY
290 Xhe skull is composed of endochondral and membra- Embryonic origin (i.e., somatic origin innervated by spina!
nous, or dermal, bones. Endochondral elements are nerves versus visceral origin innervated by cranial nerves
formed by the development of osteoblasts in cartilage provides no category for muscles that presumably are
that is formed in the chondrocranium of the larval or somatic (e.g., eye muscles) but are innervated by crania!
prehatching organism. Endochondral bones form the nerves. Insofar as possible, the following descriptions are
neurocranium and auditory capsules of amphibians, the grouped functionally in association with the appropriatc
middle ear bones, the bony portions of the hyobran- architectural unit of the skull.
chium, the jaw articulaüon, and usually the symphysis of Three types of voluntary muscles are involved with the
the lower jaw. cranium. Somatic or parietal muscles are derived em-
The more numerous dermal components form inter- bryologically from the myotomes of the epimere (i.e., the
membranously ¡n a connective üssue precursor and may dorsal píate of the mesothelial wall) and are innervatec
be categorized as investing bones of various types. Roof- primarily by spinal nerves. Somatic cranial musculature
ing and flooring bones cover the neurocranium and ol- includes the eye muscles and epaxial (dorsal) and hy-
factory capsules to varying degrees. The primary osseous paxial (ventral) muscles of the trunk that attach to th=
components of the upper and lower jaws are dermal. A back of the head and constitute the neck musculature
variety of dermal bones brace the upper jaw against, and Visceral or branchial muscles are derived embryological;.
help to suspend it from, the braincase; these bones, as from the mesoderm of the hypomere (i.e., the latera,
well as those of the jaws, invest cartilage that is derived píate of the mesothelial wall) and are innervated by dor-
from the chondrocranium. Only one dermal bone is in- sal-root homologues of cranial nerves. The latter categor.
ternal in some amphibians. This is the septomaxilla in includes some hyoid arch muscles as well as one or tuc
anurans, which is involved in protection and support of muscles that origínate on the head and insert on rhc
nasal cartilages and the nasolacrimal duct in the olfactory pectoral girdle. The remaining cranial musculature is h;.-
región. The septomaxilla is largely external in caecilians pobranchial; embryologically it is derived from myotomes
and salamanders, and there is evidence that it is of dual behind the gills that grow downward, turn forward. ar:
endochondral and dermal origin in salamanders. Anu- extend anteriorly to the jaw. Hyobranchial muscles ger-
rans are unique among amphibians in two other respects. erally are innervated by ventral-root homologues of cra-
They have fewer cranial bones and a simplified hyo- nial nerves.
branchial apparatus. A few taxa are characterized by neo- The organization of cephalic muscle descriptions is as
morphic bones that have no known homologues in other follows. The section on the neurocranium includes th£
vertebrales; all such elements described thus far are in- eye muscles, major trunk muscles of the head and nec?
termembranous in origin. región, and muscles extending between the ear and pec-
Classically, the skull and hyobranchial structure have toral girdle. Except for the eye muscles, the associatr-
been discussed relativa to the classes or origins of the of these muscles with the cranium is arbitrary and a rr.a:-
bones. But complex structures are explained more read- ter of convenience. Both cervical and ear muscles ar=
ily in terms of functional units or complexes. Accordingly, derived from somatic musculature of the trunk, but ¿VE
the following accounts are organized into discussions of actions of these muscles affect the opercular-columeDar
the bones and associated musculature of (1) the neuro- apparatus or movement of the head as a whole. More-
cranium (including the auditory capsule and middle ear over, the muscles insert on endochondral elements de-
bones), (2) the nasal capsule, (3) neurocranial investing rived from the larval chondrocranium that give rise to the
and bracing bones (including those of the auditory and adult neurocranium; thus they are described in this ur~~
olfactory capsules), (4) upper and lower jaws, (5) the Musculature associated with the nasal capsule is treatec
suspensorium, and (6) the hyobranchial apparatus. Most in that section. Muscles that open and cióse the jaws ars
details of chondrocranial structures internal to the os- described in the section on the suspensorium, and thos£
seous skull retained in adults are not discussed here but involved in swallowing and moving the hyoid and tonguc
are included in the accounts of larval structure in Chap- are treated in the section dealing with the hyobranch^a.
ter6. apparatus.
As any student of comparatíve anatomy quickly real-
izes, there is no satísfactory and totally logical way in Salamanders
which to deal with cephalic musculature. It is an anatom- Although the skulls of many species of salamanders ha~.<s
ical morass of muscles of mixed origins, uncertain hom- been described in the literature in the last 100 years. ::
ologies, and variable ñames (see Francis, 1934, for a list date no synthesis exists that summarizes the cranial ±-
of synonyms of salamander muscles, as an example). In versity of the group. Early contributions include the c-¿-
general, the following descriptions follow the nomencla- scriptions of W. Parker (1877, 1882), that of E. Emerson
ture of Edgeworth (1935). Two of the most common (1905) on the general anatomy of Typhlomolge rathbu^.
schemes of muscle descriptions are based on (1) patterns Francis's (1934) anatomical monograph on Sa/amanc-r
of innervatíon and (2) embryonic origins of the muscles. salamandra, and the works of H. Wilder (1894) anc 1
»
Musculoskeletal System
'A"ilder (1925) on plethodontids. Many useful papers were the most nearly complete, and unless otherwise specified, 291
rxiblished by students from the University of Stellenbosch the myological descriptions that follow are based pri-
r. South África. Among the most useful of these descrip- marily on that work.
~,'e papers based on histológica! preparations are Ryke
1950) on Onychodacty/us japonicus, Theron (1952) on Neurocranium. The neurocranium, housing the brain
A-nbystoma maculatum, and Papendieck (1954) on and auditory organs, extends from the posterior limits of
macrodacty/um. Less detailed descriptíons of many the nasal región to the occiput. In salamanders, the neu-
lodontids are available in Hilton (1945, 1946a, rocranium is composed of four elements, only two of
1946b). D. Wake (1963, 1966) has provided extensive which can be distínguished in the mature organism (Fig.
r.formation on plethodontids. A substantial part of the 13-1). The anterior part is the orbitosphenoid (= orbi-
recent literature deals only with particular parís of the totemporal), which probably is a parüal homologue of
íkull—for example, the sound-conducting apparatus the sphenethmoid of caecilians and anurans. The audi-
(Monath, 1965), the inner ear (Lombard, 1977), and the tory capsule is composed primarily of the prootic. Pos-
-ose (Jurgens, 1971). Paedomorphic taxa (e.g., Cryp- terior portions may arise from sepárate centers of ossifi-
:obranc/ius, Necturus) are the most frequently illustrated cation (Bonebrake and Brandon, 1971, and references
r/Aing to their use as laboratory specimens. Broader, therein), but in the adult these centers of ossification fuse
:omparative treatments are available in D. Wake (1966) with the exoccipital to form the occipital región of the
-r the plethodontids, Ózeti and D. Wake (1969) for sal- neurocranium. This posterior unit is referred to as the
smandrids, and Larsen (1963) who described some as- occipito-otic by most authors.
r^cts of the cranial osteology of neotenic and trans- Auditory apparatus.—The auditory apparatus of sal-
—rmed salamanders of a variety of taxa. Carroll and amanders is highly variable and has attracted consider-
Holmes (1980) illustrated the skulls of a number of sal- able attention since Kingsbury and Reed's (1909) original
i-nanders in their paper on the ancestry of the group. investigations. More recent contributions are those of
Lebedkina (1968,1979) contributed to an understanding Lombard (1977) on the inner ear and Monath (1965,
::" the development and evolution of the amphibian skull and included references) on the opercular apparatus. The
--.:h an emphasis on salamanders. sound-conductíng apparatus is composed of two struc-
The skulls of salamanders generally are less compact tures. The columella ( = stapes) develops first and is pre-
r.an those of caecilians and more robust than those of dominant during larval stages, whereas the operculum
— ost anurans. Dermal roofing bones are relatively small appears relatively late in the life cycle among those taxa
ir.d often few in number (Table 13-1). The temporal that possess it and, generally, is considered to be a ter-
issae are open, the orbits large, and commonly the na- restrial adaptation for sound transmission.
sal región is poorly roofed. The maxillary arcade is in- According to Monath (1965), in the generalized and
romplete, and the neurocranium poorly developed. primitive condition characteristic of some hynobiid and
The cranial architecture of salamanders is diverse and ambystomatid salamanders, the opercular apparatus
-=f.ects adaptations to a variety of terrestrial and aquatic consists of two discrete elements—an operculum and
-abitáis. columella—both of which are associated with the fenestra
The literature dealing with the cephalic myology of ovalis (= fenestra vesübuli of some authors) in the lateral
salamanders is extensive and was summarized by Francis wall of the otic capsule (Fig. 13-2). The columella is bony
1934). Work previous to this tended to concéntrate on and bears a distal stylus. The operculum is cartilaginous
romparative studies of particular muscle systems (e.g., or bony, and forms at metamorphosis in the fenestra
Walter, 1887, on visceral muscles of salamanders, anu- ovalis posterior to the columella. In both the hynobiids
rans, and reptiles; Lubosch, 1913, 1915, and Luther, and ambysiomatids, there is a trend toward reducüon or
1914, on the muscles innervated by the trigémina! nerve fusión of the operculum with the lateral wall of the otic
r. amphibians; Edgeworth, 1935, on the cephalic mus- capsule. The salamandrids exhibit a derived condition in
culature of vertebrales). Comparative studies on sala- which the columella is lost and the cartilaginous or bony
—.anders are rare and limited in scope. One example is operculum filis the fenestra ovalis. In the plethodontids,
*ie work of Drüner (1901, 1903, 1904), who compared the operculum probably is fused with the columella. The
—e muscles supplied by Cranial Nerves (C.N.) VII, IX, latter is a rod-shaped element that is fused proximally to
nd X, and the hypoglossal nerve in several species. There the operculum, which appears as a píate that filis nearly
-.as been no synthesis of the diversity of cranial muscu- all of the fenestra ovalis.
¿rure of salamanders. Because of the different ap- Muse/es of the auditory región.—Just as the bony
proaches to myological studies and the diversity of spe- structure of the opercular apparatus varíes, so do muscle
res studied (albeit limited with respect to the total diversity connections between this región and the pectoral girdle
;:' salamanders), a thorough synthesis is not attempted (Fig. 13-2). The majority of salamanders have a so-called
-.ere. Francis's (1934) account of the myology of the opercularis muscle, but this muscle is absent in some
¿eneralized, terrestrial species Salamandra salamandra is hynobiids and ambystomatids, and in all cryptobran-
MORPHOLOGY
292 Table 13-1. Probable Homologies oí Cranial and Hyobranchial Elemente in the Three Recent
Orders of Amphibians

Salamanders Caecilians Anurans

Orbitotemporal Os sphenethmoidale Sphenethmoid
[ = orbitosphenoid]
lOrbitosphenoid

process, presphenoid]
IBasisphenoid
*Dermal sphenethmoid
dermethmoid]
Occipito-otíc Os básale Otoccipital
IProotic IProotic "Prootic
lOpisthotíc !?Opisthotíc
!?Pleurosphenoid
lExoccipital lExoccipital "Exoccipital
Parasphenoid IParasphenoid 'Parasphenoid
*Columella [ = stapes] Columella [= stapes] *Columella [= stapes]
*'Operculum !?Operculum 'Operculum
*Nasopremaxilla
*Nasal •INasal Nasal
Premaxilla [= intermaxilla] IPremaxilla Premaxilla
*Septomaxilla "Septomaxilla [= turbinale, Septomaxilla [ = intranasal]
nariale]
Maxillopalatine
*Maxilla IMaxilla Maxilla
*Prefrontal *'Prefrontal
*Palatopterygoid
"Palatine IPalatíne *Palatine
Pterygoquadrate [ = pterygoid
process of quadrate]
*Pterygoid [ = palatopterygoid] ! Pterygoid Pterygoid
Palatoquadrate ! Quadrate Quadrate
*Lacrimal [= ectethmoid]
*Ectopterygoid [ = pterygoid]
IQuadratojugal *Quadratojugal
Squamosal [ = paraquadrate] Squamosal Squamosal
'* Orbital [= ocular,
postfrontal]

* = Element not present in all taxa.

! = Fused ¡n all taxa to form compound element.
" = Fused in most taxa to form compound element.
' = May be fused in a few taxa to form compound element.
? = Occurrence of center of ossificatíon questionable, or homology uncertain.

chids, amphiumids, sirenids, proteids, and the pletho- ferior (parí of the dorsal trunk musculature) inserí or. r*
dontid Typhlomolge. As Monath (1965) discussed in de- píate.
tail, there actually are two different muscles that may Eye muscles.—The eye musculaíure is composec :r
origínate from the fenestral píate; both are referred to as íhree groups of muscles. The four recti muscles hr-e
the m. opercularis and both function to transmit vibra- tendinous origins from the orbital walls of the neurocra-
tíons from the substrate and pectoral limb to the peri- nium, inserí on íhe eye, and act to turn the eyebal! r
lymph of the inner ear. In hynobüds, salamandrids, and the horizontal and vertical planes at righí angles te ~s
ambystomatids, the m. opercularis inserís on the supra- own optical axis. The mm. rectus superior, rectus inferoc
scapular cartilage and is derived from a trunk muscle, the and recíus anterior are innervated by C.N. III (OCLLO-
m. levator scapulae. In plethodontids, the m. opercularis motor), whereas the m. rectus posterior is innervated ':*.
inserts of the bony scapulocoracoid of the pectoral girdle; C.N. VI (abducens). Additional rotation of the eyeba- s
in this family, the muscle is derived from the m. cucullaris provided by the oblique muscles. The m. obliquus s_-
major, a visceral muscle of the branchial arch that is in- perior arises by a tendón from the antorbital cartilage
nervated by C.N. XI. In one plethodonüd (Pseudotñton (wall separating nasal capsule and orbit) and is inner-
montanus), parís of three muscles attach to the fenestral vated by C.N. IV (trochlear). The m. obliquus inferior
píate; the m. cucullaris major takes its origin from the also arises from the antorbital cartilage, but this muscle
píate, whereas the m. levator scapulae (a muscle of the is innervated by C.N. III (oculomotor). The two remair-
pectoral girdle) and the m. intertransversarius capitis in- ing eye muscles are the mm. retractor bulbi and levatrr
 Musculoskeletal System
293

Salamanders Caecilians Anurans

Frontal
Frontoparietal
Parietal
Vomer [ = prevomer] '* Vomer
Pseudodentary
IDentary Dentary
ISplenial
ICoronoid
!Supraangular
itetsxneckelian !Mentomeckelian *Mentomeckelian
= -nentomandibular]
Pseudoangular
¡Angular Angulosplenial [= angular,
goniale]
• L—rular ! = goniale, IPrearticular
::- ::deum]
- - - . =: ¡Articular
!?Complementale
Cearohyal [ = anterior comua Ceratohyal *Anterior cornua of hyoid
•y. hyoid]
Copula 1 [ = Basibranchial 1] Basibranchial I [ = Copula I] Copulae, hypobranchials, and
Copula II [ = Basibranchial II] Basibranchial II [ = Copula II] ceratobranchials fuse to form
hyoid píate and associated
process of anurans
ripobranchial I
"TT.pobranchial II
Ceralobranchial I Ceratobranchial I
" = Epibranchial I]
"Ceiatobranchial II Ceratobranchial II
'_ = Epibranchial II]
"Ceratobranchial III ! Ceratobranchial III
[= Epibranchial III]
•"Ceratobranchial IV ICeratobranchial IV
!= Epibranchial IV]
ICeratobranchial V

bulbi. The retractor muscle originates from the orbitos- ( = m. occipitalis), which arises from the neural spine and
menoid, inserts on the medial surface of the eyeball, and neural arch of the first vertebra and inserts over the dorsal
bears a tendinous connectíon to the eyelids. This muscle, surface of the occipital región of the skull. The third mus-
which is innervated by C.N. VI (abducens), retracts the cle, the m. intertransversarius capitis inferior, is a contin-
eyeball medially and closes the eyelids. The m. levator uation of the subvertebral trunk musculature that arises
bulbi is a thin muscular sheet that lies between the eyeball from the transverso process of the second vertebra and
and the roof of the mouth. The muscle is innervated by inserts on the ventral surface of the occiput of the skull.
C.N. V (trigeminal) and has the dual functíon of elevatíng A number of other muscles origínate on the posterior
r.e eye and thus simultaneously enlarging the buccal cavity. aspect of the skull and inserí on the pectoral girdle. Be-
Neck muscles.—Derivativos of the dorsal muscle mass cause their action involves movement of the girdle rather
m. dorsalis trunci) attach the posterior end of the skull than the head, they will be considered in the appendi-
:o the axial skeleton and provide for lateral flexión of the cular musculoskeletal system.
skull on the vertebral column. Superficially, the m. inter-
transversarius capitis superior ( = m. longissimus capitis) Nasal Capsule. The rostral región of salamanders dif-
arises from the dorsal side of the transverso processes of fers from those of caecilians and anurans in being wide
the second and third vertebrae and inserts over the pos- and usually having distinctiy separated nasal capsules (see
terolateral surface of the auditory capsule. Medial and Francis, 1934, or Jurgens, 1972, for a discussion of this
deep to this muscle is the m. rectus capitis posterior feature) (Fig. 13-1).
MORPHOLOGY
294 A premaxilla — internasal tect B prenasal proc
alary c
external naris premaxilla
obligue c
nasal narial fen
prefrontal dorsal nasal fen vomer
antorbital choana
nasolac d -¿ olfactory fen
frontal -jjf- internasal pl
maxilla—J/ orbitosphenoid
optic f
parietal
oculomotor f
pterygoid
pterygoid proc—\e
quadrate

squamosal
prootic-exoccipital
tect synoticum occipital condyle 1 —parasphenoid

orbitosphenoid- -parietal
I—squamosal
frontal- —prootic-exoccipital
prefrontal-
nasal-
nasolac d postotic f
alary c operculum
premaxilla quadrate
maxilla
pterygoid
orbitonasal f—'
—parasphenoid
vomer
i—Meckel'S c
dentar.
coronoid proc

dentary prearticular mandibular symphys 5

Figure 13-1. Skull of Salamandra salamandra redrawn from Francis (1934). A. Dorsal. B. Ventral.
C. Lateral. D. Mandible in lateral aspect and E. medial aspect. Bones are stippled; cartilage is gray.
Abbreviations: c = cartilage; f = foramen; fen = fenestra; nasolac d = nasolacrimal duct; pl = planum;
proc = process; tect = tectum.

The capsules are enclosed by the premaxillae and one another to produce an internasal cavity that contains
maxillae as well as various other dermal investing bones the intermaxillary gland. The posterior wall of each cap-
such as the vomers, nasals, prefrontals, frontals, and lac- sule is formed by a lateral, cartilaginous extensión frorr.
rimáis. The protecüon afforded by these cranial elements the orbitosphenoid bone, the lamina orbitonasalis. The
in salamanders is somewhat less than that typical of cae- roof {tectum nasi} of the capsule is fenestrate, as is the
cilians and greater than that of anurans. Thus, the carti- floor (solum nasi). The anterior end of the capsule is
laginous components of the nasal capsule tend to be formed by a cup-shaped cartilaginous structure (alary
more extensive than those of caecilians, and less well cartilage).
developed than those of anurans. The septomaxilla is Norial muse/es.—Opening and closing of the extema;
sporadic in occurrence (present in hynobiids, dicampto- naris in salamanders is controlled by three smooth mus-
dontids, ambystomatids, and many plethodontids); how- cles described by Bruner (1896, 1901). The m. constric-
ever, its absence in salamanders is not associated with tor naris arises around the posterior edge of the nana!
fusión to adjacent elements as it is in caecilians. opening and inserís on the alary cartilage anteriorly. The
The medial walls of the nasal capsules are formad by m. dilatator naris arises from a cartilaginous portion oí
the septum nasi which is synchondrotícally united with the nasal capsule posterior to the naris and extends for-
the orbitosphenoid bone. Generally, the septum is short ward to inserí on the cutaneous wall of the posterior
and thick. Anteriorly, the nasal capsule walls diverge from border of the naris. The m. dilatator naris accessorius
 Musculoskeletal System
nt in some taxa) arises from the maxilla and from Dorsal componente.—As many as five pairs of bones 295
^ge lateral to the naris and extends obliquely in an are involved in the dorsal skull roof; these are the pre-
Dmedial direcüon to inserí on the posterolateral margin frontals, nasals, and lacrimáis in the nasal región, and the
-•i naris. frontals and parietals posteriorly (Figs. 13-3, 13-4). Of
these components, only the frontals and parietals are found
in all salamanders. The frontals invest the anterior part
•crmal Investing Bones and Braces. The skulls of of the orbitosphenoid bone and in some taxa (e.g., Cryp-
: - ;- iers have unroofed temporal regions and, there- tobranchus, Salamandra, Necturus, and Siren) extend
»E- are gymnokrotaphic. However, the neurocranium forward to roof part of the nasal capsule. The paired
: • ssal capsule generally are well protected by dermal parietals lie posterior to the frontals and primarily invest
nv«síng bones. auditory capsule. In some taxa the parietal may be ex-

fasciculus fenestralis m. cucullaris major

e^ator scapulae fasciculus dorsalis of m. cucullaris major

-operculum L operculum
-:c¡umella Plethodontidae
isthmus fenestralis- 1
-m. levator scapulae superior

Salamandridae -m. levator scapulae inferior

m. ¡ntertransversarius Figure 13-2. Schematic summary

capitis inferior of conditions of ear ossicles and
associated muscles in four families of
salamanders (adapted and redrawn
Ambystomatidae from Monath, 1965). Bony elements
rcolumella are stippled. The fenestra ovalis
(= fenestra vestibuli) is black.
rfenestra vestibuli r-m. levator scapulae Dashed outlines indicate elements
r-operculum that have fused with the prootic bone
within which the fenestra ovalis lies.
Families are arranged in a primitive
to advanced sequence from bottom
to top, respectively. Among
hynobüds, the operculum always is
cartilaginous; however, in
ambystomatids, salamandrids, and
plethodontids, the operculum may be
Hynobüdae cartilaginous or bony.
MORPHOLOGY
296
A

oper

orbsphen
vom
quad

oper

pmax

ope

Figure 13-3. Dorsal (left) and ventral (right) views of salamander skulls. A. Salamandrella keyserlingii.
B. Cryptobranchus alleganiensis C. Rhyacotriton olympicus. D. Ambystoma maculatum. E. Tarícha
granulosa. F. Amphiuma means. G. Pseudobranchus srriarus. Skulls are not drawn to relative scale.
Stippled pattern indicates cartilage; dorsal fenestrae are hatched. Cartilaginous pterygoid processes are not
shown. A, B, E, and G redrawn from Larsen (1963), C from Cloete (1960), D from Theron (1952), and F
from Erdman and Cundall (1984). Abbreviations Usted in Fig. 13-4.
 Musculoskeletal System
I laterally over the cxoccipital and prootic to artic- maxilla against the central part of the skull. The nasal is 297
• Á-ith the squamosal (e.g., Hynobius, Batrachuperus, variable in its configuration and association with adjacent
urna, Salamandra, and Cryptobranchus, but not bones (Figs. 13-1, 13-3, 13-4). In Siren, the nasal is long
s. Ambystoma, or Notophthalmus). and slender, and lies medially adjacent to the alaty process
are present in all salamanders except the pro- of the premaxilla; thus, it provides only a minimal roof
JVecturus and Proteus) and some plethodontíds to the olfactory capsule and braces the premaxilla, in-
Haideotriton and Typhlomolge). Loss of this ele- stead of the maxilla, against the skull. The nasals always
i» presumed to be an expression of paedomor- lie anterior to the prefrontals (if present) and the frontals;
When present, the nasal roofs the nasal capsule however, their relationship with the alary processes of
ir. associatíon with the prefrontal, helps to brace the the premaxillae is variable. In primitive taxa, such as

vom

pter proc

vom tooth
patch

quad

Figure 13-4. Dorsal (left) and ventral (right) views of plethodontid salamander skulls. A. Phaeognathus
•mbrichti. B. Stereochilus marginatum. C. Plethodon jordani. D. Bolitoglossa subpalmata. E. Bolitoglossa
hortwegi. f. Eurycea neotenes. Stippled pattern indicates cartilage; dorsal fenestrae are hatched.
A—D redrawn from D. Wake (1966), E from D. Wake and Brame (1969), and F from Larsen (1963).
Abbreviations: col = columella; exoc = exoccipital; fron = frontal; lac = lacrimal; max = maxilla; ñas =
nasal; oper = operculum; orbsphen = orbitosphenoid; pal-pter = palatopterygoid; par = parietal; pfron -
prefrontal; pmax = premaxilla; pro = prootic; pro-exoc = prootic-exoccipital; prsph = parasphenoid;
pter = pterygoid; pter proc = pterygoid process; quad = quadrate; spmax = septomaxilla; sq =
- luamosal; vom = vomer; vom tooth patch = vomerine tooth patch.
MORPHOLOGY
298 Cryptobranchus and Hynobius, the nasals articúlate with metamorphosed plethodontids (Fig. 13-4) and large Si-
one another medially and lie posterior to the premaxillae, ren. The pterygoid articúlales with the inner side of the
whereas in more advanced taxa (e.g., Salamandra, Nec- quadrate and the anterior wall of the prootic posteriorly
turus, Amphiuma, Ambystoma, and some of the pleth- An anterior ramus extends forward to, but does not bear
odontids), the nasals are separated medially by the alary a bony articulation with, the posterior end of the maxilla
processes of the premaxillae. In the proteiid Necturus, which lacks a maxilla, the pter-
The prefrontal is a small bone located at the anterior ygoid bears teeth, articúlales with the vomer, and func-
margin of the orbit, usually in articulation with the nasal tionally forms the posterior half of the upper jaw.
and frontal (Fig. 13-1). Prefrontals are present in all sal- Lateral component.—The squamosal is present in aE
amanders except the sirenids, proteids, and some pleth- salamanders (Fig. 13-1). The bone articulates either with
odontids (Fig. 13-4); loss in these groups is thought to the posterolateral edge of the parietal or with the proot:
be paedomorphic. When present, the bone forms part of bone and invests the quadrate laterally.
the roof of the nasal capsule and acts with the lacrimal
(if present) to brace the maxilla against the frontal. In the Upper and Lower Jaws. In most salamanders, the
absence of a lacrimal bone, the prefrontal bears a groove upper jaw is composed of a premaxilla (paired or un-
or tube that supports the nasolacrimal duct. paired) anteriorly and paired maxillae posteriorly (F:c
The lacrimal is present only in the hynobiids and di- 13-1). These dermal bones are dentate in all taxa, excep:
camptodontids (Fig. 13-3). The bone forms part of the the sirenids, most Thorius and some Bolitoglossa.
anterior margin of the orbit, thereby bracing the maxilla Premaxilla.—The premaxillae (= intermaxillae of sorné
against the prefrontal. A tube in the lacrimal endoses the authors) are paired in all transformed and nontrans-
posterior part of the nasolacrimal duct. formed cryptobranchids, ambystomatids, proteids, an;
Ventral componente.—Salamanders have three ven- sirenids. Among the remaining salamanders, the pre-
tral investing bones—paired vomers anteriorly and a me- maxillae may be sepárate (e.g., Ambystoma, most hy-
dian parasphenoid posteriorly (Fig. 13-1). Generally, the nobiids, and some plethodontids) or fused (Figs. 13-3.
vomers are large palatal bones that lie adjacent to the 13-4), as in one hynobiid (Hynobius nebulosus) and mar/,
premaxillae and maxillae anteriorly (except in Necturus, salamandrids and plethodontids (e.g., Tañería, Batrachc-
in which the vomer functionally forms part of the upper seps, and Eurycea). In Amphiuma (Fig. 13-3A), the pre-
jaw). The posterolateral margin of each vomer usually maxilla arises from a single center of ossification. T-.Í
forms the bony margin of the interna! choana, and the premaxilla is composed of three parís. The primary corr.-
vomer, as a whole, floors the nasal capsule. The rela- ponent of the premaxilla that is involved with the max-
tionship of the vomer to the parasphenoid is highly var- illary arcade is the tooth-bearing pars dentalis ( = pan
iable. The bone overlaps the anterior part of the paras- alveolaris of some authors). The dorsal ramus that arises
phenoid to some degree in all taxa, and depending on from the pars dentalis to form a skeletal roof and anterior
the configuration of the vomerine teeth, may have an abutment for the nasal capsule is termed the pars praer.-
attenuate dentigerous process that extends nearly the en- asalis (= pars dorsalis, pars frontalis, frontal spine. •:•:
tire length of the parasphenoid (e.g., some plethodon- alary process of some authors). These portions of the
tids). premaxillae are highly variable in size among salaman-
The parasphenoid invests the braincase ventrally and ders; they may be small (as in most hynobiids) or laige
is present in all salamanders. Although usually it is broader (e.g., Ambystoma maculatum). The processes are adja-
in the prootic región than ¡n the orbitosphenoid región, cent to one another ¡n some taxa (e.g., Ambystomai zi
the parasphenoid usually lacks distinct posterolateral alae. separated. The pattern of separation also is variable. F:r
Unlike the parasphenoid bones of caecilians and some example, the partes praenasali are separated by the r.=-
anurans, the parasphenoid of salamanders is not incor- sals in Salamandrella keyserlingn and by the frontals r
porated into the ossification of the braincase. Salamandra salamandra. Among the plethodontids. th;
The morphogenesis and development of the two re- partes are separated by a so-called fontanelle in some
maining palatal elements—the palatine and pterygoid— taxa (e.g., Plethodon cinereus), whereas in others r.£
are controversia!. Mostauthors (e.g., Larsen, 1963) seem partes are fused distally (e.g., Desmognathus and Stere-
to think that the centers of ossification of the palatine and ochilus) to endose the fontanelle. The third portion r:
pterygoid are Consolidated to form a single palatoquad- the premaxilla is the pars palatina, a ledge of bone alone
rate bone, but Lebedkina (1960) reported that the two the lingual side of the pars dentalis. The pars palatina is
bones begin to ossify separately in Hynobius and Pleu- absent in proteiids, sirenids, and neotenic plethodonticií;
rodeles but fuse soon after their appearance. Whatever it is poorly developed in cryptobranchids, amphiumics
the case, the palatine functionally is lost ¡n all adult sal- and ambystomatids. Among the remaining taxa, it forms
amanders, except Siren and Pseudobranchus (Fig. the anterior part of the bony palate, but varíes from smal
13-3), in which the bone is a small, quadrangular element to large in size.
lying posterolateral to the vomers near the anterior end Maxilla.—In most salamanders, the maxilla completes
of the parasphenoid. The pterygoid (palatopterygoid of the upper jaw laterally (Fig. 13-1). It is absent in the
some authors) is present in all salamanders except fully proteiids, Pseudobranchus, and Typh/omo/ge, vestigial L-.
 Musculoskeletal System
i reduced or sometimes absent in other pae- Suspensorium. The suspensory apparatus is a com- 299
: species (Fig. 13-3). As with the premaxilla, plex of cartilaginous, bony, and muscular elements that
:i:t of the maxilla is the pars dentalis. Along act to suspend and brace the jaws against the central part
: r margin of the bone, there is a vertical process of the skull, and owing to muscle origins and insertions
í the pars facialis that forms the lateral wall of enable the organism to open and cióse the mouth.
capsule. The lingual pars palatina is variably Skeletal componente.—The central element of the
; among different species and, when present, apparatus that suspends and braces the jaws against the
-. í medially with the vomer. The posterior end of skull in salamanders is the palatoquadrate, which lies nearly
_2 bears ligamentous connections with two ele- perpendicular to the long axis of the skull and is deflected
-r-.e quadrate and the pterygoid. in an oblique, downward direction (Fig. 13-5). The pal-
Mmitdible.—Basically, the mandible of salamanders atoquadrate consists of two major parts, a dorsal or prox-
::' two dermal bones that invest Meckel's carti- imal cartilaginous portion, known as the pars quadrata,
: i of cartilage that extends the length of the jaw, and a ventral or distal part that is the ossified quadrate.
".es anteriorly as the mentomeckelian (= men- The quadrate is situated dorsal to the pars articular, the
rular of some authors), that forms in Meckel's cartilaginous área that articúlales with the lower jaw, or
.n the área of the mandibular symphysis (Fig. the ossified articular if present.
~-.e tooth-bearing portion of the lower jaw is the Proximally, the pars quadrata bears three cartilaginous
• -. and the coronoid in the proteid NectumsJ. The connections with the auditory capsule. These connec-
5 synostotically united with the mentomeckelians tions are arranged in a tripod-like fashion so that a cavity
. and extends along the lateral and ventral sur- with three exits is enclosed between the palatoquadrate
Meckel's cartilage. The lingual side of Meckel's and the auditory capsule. The dorsal process lies beneath
.- ;:; :s invested by the prearticular ( = gonial or co- the squamosal and is known as the otic process. It is
.-^.c¿um of some authors). The prearticular is elabo- synchondrotically united (i.e., fusión of two cartilaginous
in the articular región to form a coronoid flange structures) with the crista parotica of the otic capsule in
.- •;- spproximates the pterygoid and serves for the at- most taxa, although the connection is reduced or lost in
r.: - -;-.t of masticatory muscle fibers. Posteriorly, in the some (e.g., Cryptobmnchus and Rhyacotríton). The as-
-:. i: región, part of Meckel's cartilage may ossify as cending process is anterior and ventral to the otic process
-: ;—rular. Cryptobranchoids have an angular bone in and is fused to the otic capsule. The third and largest
-: - "dible, and most paedomorphic salamanders have process is the basal process which lies directly ventral to
: ::--bearing coronoid. Adult Dicamptodon have an the otic process. The basal process is fused completely
:-".iie coronoid. with the larval skull and remains so in adults of most
Dentition.—The teeth of most salamanders are short salamanders (e.g., Triturus, Salamandra, and Pletho-
-: bicuspid (Fig. 15-20A). However, in a few male don), although in some species the basal process is sep-
-:~.odontids the maxillary teeth are elongate, mono- arated from the auditory capsule by an outgrowth of con-
-•~'.d. and directed anteriorly; in some species of Eu- nective tissue (e.g., Ambysíoma maculatum and
:~z the teeth of both jaws are elongated and mono- Hynobius). Because this separation occurs slightly lateral
-;r:d. Replacement teeth on the jaws and all other to the point of original fusión, a portion of the primitive
::hed elements are formed interior to the older rows basal process remains fused to the auditory capsule. The
- :=3th; the replacement teeth move peripherally to re- basitrabecular process (or secondary basal process) is
;:e older teeth as they are resorbed (Regal, 1966; Law- connected to the skull by a joint—a condition generally
:-. etal., 1971). characterizing primitive salamanders. In addition to these

rproot¡cf
rprootic

r-fen ovalis
ascending proc exoccipital
postotic f
r'bitosphenoid

optic &oculomotor f columella

pars quadrata
pterygoid proc-
cranioquadrate passage '
Figure 13-5. Palatoquadrate and suspensorium
basal proc of the dicamptodontid salamander Rhyacotríton
otic proc ceratohyal olympicus. redrawn from the graphic
reconstruction of Cloete (1961). Abbreviations:
f = foramen; fen = fenestra; proc = process.
MORPHOLOGY
300 synchondrotic connections and articulation, the pars The antagonist of the levator mandibulae series is íhe
quadrata is attached to the sound-conducting apparatus m. depressor mandibulae, which is innervated by C.N.
by the suspensorio-columella ligament. VII (facial) and acts lo open the jaw. This muscle origi-
In adult salamanders, the palatoquadrate bears a fourth nales from the posterior part of the squamosal, the au-
process at its dista! end, the pterygoid process. This process ditory capsule, and the superficial dorsal fascia of the
arises from an independent chondrification but is contin- head and shoulder, and inserís on the posterior end of
uous with the palatoquadrate of the adult, where it pro- the mandible at its articulation with the quadrate (Fig.
trudes from this element in an anterolateral direcüon to- 13-6). The origin of íhe m. depressor mandibulae is var-
ward the posterior end of the maxilla. The pterygoid iable among íaxa; moreover, il may become separatec
process is overlain by the pterygoid in all taxa except into superficial and deep parís, or anfero- and posíero-
adult plethodontíds which lack the pterygoid. laíeral parís.
Two dermal investing bones, the pterygoid and the
squamosal, are associated with the palatoquadrate (Figs. Hyobranchial Apparatus. The hyobranchial appa-
13-1, 13-3, 13-4). Although adult plethodontíds lack a raíus consisís of íhe hyobranchial skelelon, which lies ir.
pterygoid, in all other salamanders this bone extends from íhe floor of íhe mouíh and serves as a síruclural base ice
the posterior end of the pars quadrata toward the maxilla. the tongue. The hyobranchium bears muscular and liga-
A groove in its dorsal surface accommodates the carti- mentous attachmenls 1o íhe lower jaw, skull, and pectora.
laginous pterygoid process. The bony pterygoid does not girdle.
articúlate with the maxilla. The squamosal invests the Skeletal componente.—In mosl adult salamanders. rts
palatoquadrate laterally and articulares with the crista hyobranchial apparatus consiste only of porrions of "•€
parotíca of the prootíc and, in some salamanders, the hyoid and íhe firsl two branchial arches, íhe remainóer
parietal dorsally. having disappeared during melamorphosis. Although ±>£
Suspensory máseles.—The primary muscles respon- configuralion of íhe hyobranchium varíes consideraba,
sible for the opening and closing of the jaws are the mm. among salamanders (Fig. 13-7), íhe basic struclure is as
levator (= adductor) mandibulae and depressor man- follows. Usually Ihere is one medial, longiludinal elen-err
dibulae, both of which are visceral muscles (Fig. 13-6). lermed íhe copula or basibranchial, lo which olher pars
The adductor musculature is a complex of mandibular of íhe hyobranchial apparalus are attached. Some pae-
arch muscles that are innervated by C.N. V (trigeminal), domorphic salamanders such as Proteus and Siren h.a-.«
arise from the skull roof and inserí on the lower jaw, and íwo median elemente. Anlerolalerally, íhe copula usualn.
act to elévate or cióse the lower jaw. Variation in this bears a pair of horns (also lermed anterior radiáis! ±a:
muscle complex was discussed by Carroll and Holmes are imbedded in íhe longue musculalure. In an anterior
(1980). The m. levator mandibulae is composed of two to posterior sequence, íhe copula(e) is flanked by ~«E
major muscle masses—the mm. levator mandibulae an- following pairs of elemente: íhe ceralohyals and one or
terior (= internus) and levator mandibulae externus. The two pairs of hypohyals. The ceratohyals (anterior comua
m. levator mandibulae anterior lies medial to the man- of íhe hyoid) usually are relatively massive elements e*-
dibular branch of C.N. V and is divided into superficial cepl in íhe plelhodontids) Ihal lie veníral lo íhe h;,pc-
and deep layers. The superficial portion arises from the branchials and curve dorsally from Iheir medial artir^fr
skull roof and the dorsal fascia that extends from the skull tion wilh íhe copula toward the suspensorium. The
to the neural spine of the first vertebra; the muscle then ceralohyals bear a ligamenlous connection wilh íhe sus-
traverses the otic región and extends ventrally anterior to pensorium dislally. The hypobranchials may be Ihc-ugr
the auditory capsule to inserí via a tendón on the coro- of as connecting rods belween íhe copula medially an¿
noid process of the mandible. The deep portion of fhe íhe ceralobranchials dislally.
m. levator mandibulae aníerior is a fan-shaped muscle Il seems useful lo inserí a parenlhelical slalemen: haz
that originales from íhe skull roof and inserís on íhe dor- regarding íhe use of íhe lerms ceralobranchial ar.c ¿p-
sal margin of íhe mandible just anterior to the jaw artic- branchial for íhe terminal elemente of íhe posterior brar-
ulation. The m. levator mandibulae posterior arises from chial arches in salamanders. In íhe lileralure dealing wiÉ
the squamosal, quadrate, and pterygoid to a fleshy in- plelhodonüd salamanders beginning with WiedersheiB
sertion on the articular portion of Meckel's caríilage and, (1877), continuing through H. Wilder (1894) and L WUm
via a tendón, on the coronoid process just anterior to the (1925), and culminating wilh the many recent contrib»-
insertion of íhe superficial parí of the m. levator mandi- tions by D. Wake and his colleagues, the ceralobrancraas
bulae aníerior. The fourth parí of íhe levator musculalure have been referred to as epibranchials. Use of tris ~c-
is íhe m. levator mandibulae externus which lies anterior menclalure is based on fhe inlerprelation Ihal the hyo-
to the m. levator mandibulae posterior and laíeral fo íhe branchial and ceralobranchial elemente of fishes are rq
trigeminal nerve. The muscle originales from íhe squa- resenled by only one element in salamanders. a booe
mosal and anterior wall of the auditory capsule and in- termed íhe ceralobranchial. Dislal elemente then ae
serís on the posterior end of the dentary and lateral sur- termed epibranchials. If one assumes thal epibranc~-as
faces of the coronoid process of the mandible. are losl in amphibians and olher letrapods [allhougr. Es-
 Musculoskeletal System
i—lev mand ext 301
dp lev mand ant sp lev mand ant
pfron-i
fron -intermyo epax

-lev mand ext

-ant dep mand

-post dep mand

¡nterhyoid post
"and ant
dent—l
intermand post

interhyoid ant

i—sp lev mand ant

[—intermyo epax
dp lev mand ant— r— spir lig
ptermax liq

basibran

hyomand lig 1 —rect cerv

hypobran- —cbran I
hyoquad lig—' —ceratohyal

Frgnre 13-6. Cranial musculature of Amphiuma tridactylum in lateral view. A. Superficial. B. Deep.
Redrawn from Erdman and Cundall (1984). Abbreviations: ant dep mand = m. depressor mandibulae
interior; basibran = basibranchial; cbran I—IV = Ceratobranchials I—IV; dent = dentary; dp lev mand
¡oí = deep m. levator mandibulae mandibulae anterior; fron = frontal; hyomand lig = hyomandibular
rament; hyoquad lig = hyoquadrate ligament; hypobran = hypobranchial; interhyoid ant =
m. interhyoideus anterior; interhyoid post = m. interhyoideus posterior; intermand ant = m.
i-.termandibularis anterior; intermand post = m. intermandibularis posterior; intermyo epax = m.
irttermyoseptal epaxial; lev are I—IV = mm. levatores arcuum I—IV; lev mand ext = m. levator mandibulae
externus; max = maxilla; ñas = nasal; pfron = prefrontal; pmax = premaxilla; post dep mand = m.
iepressor mandibulae posterior; pro = prootic; proc = process; ptermax lig = pterygomaxillary ligament;
rect cerv = m. rectus cervicis; sp lev. mand ant = m. levator mandibulae anterior superficialis; spir lig =
-acular ligament; sq = squamosal; subarc rect I, II, IV = m. subarcualis rectus I, II, or IV.
MORPHOLOGY
302

chyal

bhyal
hhyal
-bbran I
corp a-:
V-chyal
-*— hbran
hbran
cbran I

cbran II-IV

ant rad
are
post rad

<lSs£
I—bbran I
— chyal

Figure 13-7. Hyoid apparatus of some representative salamanders. A. Cryptobranchus allenganiensis,

ventral view. B. Salamandra salamandra, ventral view. C. Rhyacotriton olympícus, dorsal aspect.
D. Proteus anguinus in ventral and E. lateral views. F. Ambystoma macrodactylum, dorsal view. G. Aneides
sp., ventral aspect. Drawings adapted from following sources: A—Jollie (1962); B—Francis (1934); C—Cloete
(1960); D—E—Marche and Durand (1983); F—Papendieck (1954); G—Hilton (1947). Abbreviations: ant
rad = anterior radius; bbran I—II = Basibranchials I—II; bhyal = basihyal; cbran I—IV =
Ceratobranchials I—IV; chyal = ceratohyal; corp are = corpus arcuata; hbran I—II = Hypobranchials I—
II; hhyal = hypohyal; post rad = posterior radius; rad = radius.

ton (1933) suggested that an epihyal might be present Siren) fusión usually is evident; thus in Siren, Cerato-
between the ceratohyal and its connection to the pala- branchials II-IV are fused proximally and articúlate witr.
toquadrate in Ambystoma macrodactylum], then ¡t fol- Hypobranchial II. Some taxa (e.g., most plethodonticis
lows that the terminal hyobranchial elemente of sala- and Proteus) develop only three branchial arches insteac
manders would be Ceratobranchials. For the time being, of the usual four, thereby eliminaflng the possibility c:
this issue is unresolved, but the term Ceratobranchials is having four pairs of Ceratobranchials. In the majority of
used in this text. salamanders, the Ceratobranchials are either fused or los:
Usually there are two pairs of hypobranchials and be- so that only one distal element remains to articúlate with
tween one and four pairs of Ceratobranchials. Reduction the ends of Hypobranchials I and II.
by loss and/or fusión of the posterior elemente of the Hyobranchial máseles.—The musculoskeletal system
hyobranchial apparatus is common among salamanders. of the hyobranchial apparatus ¡s complex. The muscles
Necturus, Proteus, and Amphiuma, as examples, have and bones of the floor of the mouth are involved in ven-
only one pair of hypobranchials. Most salamanders show ülation and in feeding, which involves the complete cycle
some degree of reduction in the number of Ceratobran- of procuring prey, manipulating food in the buccal cavity.
chials. If four pairs are present (e.g., Pseudobranchus and and then swallowing it. Capture of prey is accomplishec
 Musculoskeletal System
one of several mechanisms (see Chapter 9), depend- salamanders such as Cryptobranchus and Amphiuma. 303
an the age of the salamander and on the species. Plethodontid salamanders lack a larynx and all laryngeal
the musculoskeletal system of a gape-and-suck muscles. A superficial sheet of musculature lies between
• such as the neotenic Necturus would be expected the rami of the lower jaw (Figs. 13-6A, 13-8A). The an-
¡ considerably different from that of terrestrial feeders terior part of this sheet is the m. intermandibularis, sup-
sscr. as Salamandra and Bolitoglossa, which use their plied by C.N. V (trigeminal); the posterior part of the
mangues to obtain food. In some plethodontids (e.g., Hy- sheet is the m. interhyoideus that originales mainly by a
; -.res], the salamanders are able to project the tongue tendón from the quadrate. Contraction of the m. inter-
rbcyond the mouth (Fig. 9-5); this ability depends on mandibularis results in elevation of the floor of the buccal
s -Dghly derived and specialized hyobranchial complex. cavity. Contraction of the anterior part of the m. inter-
hyoideus (innervated by C.N. VII, facial) constricts the
Laryngeal and swallowing muse/es hyobranchial skeleton and the posterior part of the mouth.
Tr.e principal muscles used in swallowing are the mm. Actíon of the posterior part of the m. interhyoideus con-
ator laryngis, constrictor laryngis, intermandibularis, stricts the pharynx, and depresses the head and moves
lyoideus, cephalodorsosubpharyngeus, and levator it sideways. The m. levator bulbi is a sheet of muscle
The mm. dilatator laryngis and constrictor laryngis lying between the eye and the roof of the mouth. Inner-
antagonistíc muscles innervated by C.N. X (vagus) vated by C.N. V (trigeminal), this muscle contraéis to
: open and cióse the larynx and glottis. The dilatator raise the eye, thereby enlarging the buccal cavity. The
i single, arising from the hyobranchial skeleton and in- m. cephalodorsosubpharyngeus is supplied by C.N. X
- g on the arytenoid cartilage. There may be two sets (vagus) and derived from gilí muscles of the larva. It arises
a constrictors—the constrictor laryngei dorsalis, anterior from the posterolateral área of the skull and passes ven-
•n ríe insertion of the dilatator, and the c. laryngis, pos- trally between the m. depressor mandibulae and the m.
snor to the insertion. The c. laryngei dorsalis is lost at cucullaris to insert along the midline dorsal to the pharynx
TDeamorphosis in some salamanders such as Salaman- anterior to the larynx. Contraction of this muscle causes
a-= and Trituras, but apparently is retained in all neotenic constriction of the pharynx.

mand

subhyo

i-ossa-quad
gemohyo
rect cerv sp

quadpect heboypsil Figure 13-8. Throat muscles of the

subarc rect rectcerv pf salamandrid Chiogiossa ¡usitanica.
A. Superficial musculature. B. Deep
basirad rect longitudinal muscles. C. Deep
cerv sp muscles of hyobranchial apparatus.
omohyo Nomenclature follows Ózeti and
D. Wake (1969) from whom drawing
radius is adapted. Abbreviations: basibran
basibran I I—II = Basibranchials I—II;
ceratohyal basirad = m. basiradialus; geniohyo
= m. geniohyoideus; heboypsil = m.
hebosteoypsiloideus; imand post =
m. intermandibularis posterior;
i-ossa-quad = m. interossa quadrata;
mand = mandible; omohyo = m.
basibran omohyoideus; quadpect = m.
quadratopecoralis; rect cerv pf = m.
rectus cervicis profundus; rect cerv sp
= m. rectus cervicis superficialis;
subarc rect = m. subarcualis rectus;
—sternum subhyo = m. subhyoideus.
MORPHOLOGY
304 Mm. rectas cervicis and geniohyoideus pula or basibranchial. The effecí of íhis combined actior
Movement of the hyoid and tongue is affected by a is to project íhe íongue forward and ouí of íhe rnour
complex of muscles, some of which are derived from the (see discussion of íhis mechanism in Chapíer 9).
ventral trunk musculature (Figs. 13-6A, 13-8A, 13-8B).
The m. rectus cervicis, an anterior continuation of the m. Mm. genioglossus and hyoglossus
rectus abdominis, is divisible into superficial and deep The tongue is composed of the m. genioglossus (ab-
layers that arise from the sternum. Because the m. rectus sent in at leasí Siren and Pseudotríton) and the m. hyo-
abdominis profundus bypasses the sternum in pletho- glossus, both of which are innervated by íhe hypoglossa.
dontíds, the m. rectus cervicis profundus is a direct con- nerve. In mosl salamanders íhe bulk of íhe íongue s
tinuation of this muscle. Both portions are innervated by made up of íhe m. genioglossus which originales frorr.
the first three spinal nerves. The deep portion inserís on íhe mandibular symphysis and consiste of lwo parte. A
the dorsal side of the copula or basibranchial of the hyoid medial bundle of parallel fibers inserte in íhe base of thc
in some taxa, but the usual insertion ¡s into the substance tongue and in a ligamení íhal also connecls lo íhe basi-
of the tongue pad. The superficial part is a broad sheet branchial of íhe hyoid and íhe insertion of íhe deep por-
of muscle that passes dorsal to the coracoid to inserí on tion of íhe m. recíus cervicis. The second part consiste o:
the ventral surface of íhe hyoid. The m. recíus cervicis a fan-shaped group of fibers thal spread oul over the
relracís íhe hyoid and, íherefore, íhe íongue. The m. floor of íhe moulh, where Ihey inserí al íhe sides of the
geniohyoideus is a slrap-like muscle thal lies deep lo íhe tongue. The fibers of íhe m. hyoglossus arise from thc
m. intermandibularis. In some taxa (e.g., species of Sal- dorsal surface of íhe hyoid and exlend inlo íhe íongue
amandra, Trituras, Eurycea, Pseudotríton), fhe m. gen- (Fig. 9-6). The projectile longues of some salamandrics
iohyoideus also has a laleral componenl thaí originales and plelhodonlids are possible because of consideraba
from the inner edge of the lower jaw anteriorly and inserís modificarion of íhe hyobranchium (see Chapíer 9).
on the ceratohyal posíeriorly. lis insertion is associated
wiíh the anterior end of íhe m. recíus cervicis. The m.
geniohyoideus is innervaled by íhe hypoglossal nerve; Caecilians
contraction of íhis muscle depresses íhe lower jaw or íhe Caecilians have remarkably compací, well-ossified skuls
eníire head if íhe jaws are kepl closed by íhe masíicatory thal are slegokrotaphic (skull complelely roofed excepc
muscles, and pulís íhe hyoid apparatus forward. The m. for narial, orbital, and lenlacular openings) or zygokr:-
íransversus ventralis is a deep branchial muscle, inner- laphic (presence of a zone of weakness or a narrow •:-
valed by C.N. X (vagus), and originating from íhe ter- nelic sulure belween íhe squamosal and parielal bor.es
minal ceratobranchial and inserting on a median raphe. in the temporal región). The temporal regions of motf
In some salamanders (e.g., Pseudotríton), the muscle forms anurans and salamanders are unroofed, a condition re-
the subpharyngeal part of the m. cephalodorsosubphar- ferred 1o as gymnokrolaphic. The origin of the solid>.
yngeus. roofed skull in caecilians has been a focal point of cor-
tinued conlroversy regarding íhe origins of the grouz
Mm. subhyoideus and subarcualis rectus I Some individuáis consider caecilians to have been óe-
Two deep visceral muscles are associaíed wiíh tongue rived secondarily from an ancestor wilh a reduced sk_l
movemení (Fig. 13-8B). The m. subhyoideus (absení in lypical of other Recent amphibians, whereas others favor
ambysíomatids and plelhodonlids) is supplied by C.N. íhe idea of a caecilian descent from Paleozoic microsatrs
VII (facial) and arises from íhe posterior end of íhe cer- The most receñí reviews of these conflicting hypolhess
afohyal and inserís on íhe dorsal surface of íhe aponeu- can be found in Carroll and Curie (1975), Nussbairr
rosis of the m. intermandibularis. When the muscle con- (1977, 1983), and M. Wake and Hanken (1982). Despile
íracts, the dorsal margin of the ceratohyal is deflecled íhis débale, Ihere is consensus íhal íhe configuratior. cr
anlerovenlrally and íhe íongue above is elevaled. The íhe caecilian skull is associaíed wilh funclional demar.z
m. subarcualis recíus I (Fig. 13-6B), innervated by C.Nn. imposed by Iheir fossorial mode of exislence. Earlier x-
IX and X, arises from íhe dorsal side of the posterior end scriplions of caecilian skulls are ciled by M. Wake are
of the first ceratobranchial caífilage. The muscle arises Hanken (1982). The only broad comparalive treatmerr
from a pinnaíe raphe from which fibers radíale around is thal of E. Taylor (1969). Perusal of the latler and i
the end of íhe caríilage ío endose it in a muscular cup roll and Curie's (1975) summary documente variation i
and íhen inserís on íhe aníerovenlral border of the cer- íhe numbers of dermal invesling and bracing bones ow-
aíohyal. The action of the m. subarcualis complemenís ing 1o apparenl fusión of elemente. Because of the lac*
íhaí of fhe m. subhyoideus. Thus, íhe m. subhyoideus of comparalive developmenlal dala (only Dermophs
roíaíes and secures íhe anterior element of íhe hyoid mexicanus is well documenled by M. Wake and Hanken.
(ceratohyal), thereby elevaling the tongue slightly. Con- 1982), íhe homologies of cranial elemente among cae-
traction of the m. subarcualis rectus I pulís the posterior cilians are somelimes queslionable; íhe homologies of
end of the firsí ceratobranchial venlrally while forcing íhe many caecilian cranial componente wilh ihose of sala-
branchial arches ío roíate forward abouí íhe median co- manders and anurans conslilute a subjecl Ihat has yel lo
 Musculoskeletal System
;áressed. As a consequence, the terminology of os- nethmoid in the adult (Table 13-1)—the orbitosphenoid 305
y*^ elements among the groups frequently is incon- áreas laterally, the mesethmoid (or prenasal process) an-
5=Tí-.: and confusing. A provisional scheme of equivalen! teromedially, the basisphenoid ventromedially, and the
: :s presented in Table 13-1. supraethmoid dorsomedially. The sphenethmoid is ob-
T"-.€ literature dealing with cephalic musculature of scured ventrally and laterally by dermal investing bones,
> was reviewed by Bemis et al. (1983). Among but its dorsal exposure varíes. In some species (e.g., Hy-
:: ks that include comparisons with other amphibi- pogeophis rostratas, Scolecomorphus u/uguruensisj, the
:•-: Luther (1914). Edgeworth (1935), and Nishi bone is covered completely (Figs. 13-9, 13-10), whereas
L.ro¿ . Descriptive morphology is provided by Wieder- in others (e.g., Schistometopum thomensis, Idiocranium
- 1379). H. Norris and Hughes (1918), de Jager russe/i) the dorsomedial, or supraethmoidal porüon, of
l?59a. 1939b), andLawson (1965). Bemis et al. (1983) the bone is exposed and sometimes termed the infra-
ice Nussbaum (1983) were the first authors to provide frontal or dermethmoid.
tacnonal analyses and/or interpretations of the cranial The posterior braincase, the os básale, is represented
: f oí caecilians. The former work is especially useful by a unit of complex origins—the exoccipitals, posteriorly,
• . --: :he authors presented a provisional list of syn- the otic capsules laterally, and the parasphenoid ven-
•KTTIS of cephalic muscles. trally—all of which are synostotically fused in adults. The
exoccipitals ossify in cartilage around the foramen mag-
Searocranium. The caecilian braincase is composed num and form the occipital condyles and posteromedial
jt r*o complex units—the os sphenethmoidale anteriorly walls of the auditory capsule. The remainder of the au-
te. anterior to the optic foramen) and the os básale ditory capsule also is endochondral in origin. M. Wake
acsreriorly. In the adult, the sphenethmoid is a single and Hanken (1982) reported that ossification aróse from
bone that houses the anterior end of the brain and forms a single center (? the prootic) in Dermophis, but earlier
tt medial, posterior, and posterolateral walls of the nasal workers (summarized in De Beer, 1937) recorded as many
capsule. The bone is endochondral in origin and formed as three sepárate centers of ossification (prootic, opis-
fcom five ossification centers, the ñames of which fre- thotic, and pleurosphenoid) in other caecilians. Ventrally,
iy are used to desígnate various parts of the sphe- the parasphenoid, an investing bone of membranous or-

ext naris
naspmax

vomer
maxpal
choana
frontal

parietal
-sq-
columella
pterquad
os básale
occipital condyle car f
frontal—i sq
naspmax—\ _ parietal
ext naris os básale
columella
Figure 13-9. SkulI of Dermophis
mexicanus. A. Dorsal. B. Ventral.
maxpal -orbit I— pterquad C. Lateral. D. Mandible ¡n lateral
view and E. medial view. Redrawn
from M. Wake and Hanken (1982).
Abbreviations: car f = carotid
foramen; maxpal = maxillopalatine;
naspmax = nasopremaxilla;
retroart p pterquad = pterygoquadrate; retroart
p = retroarticular process; sq =
- pseudoangular- squamosal; tent f = tentacular
• pseudodentary- foramen.
MORPHOLOGY
306 pmax-
spmax
nasal
vomer
maxpal

orbít

parietal
pterquad
os básale
quad columella —
os básale
occipital condyle-
frontal parietal
nasal
spmax
ext naris os básale
Figure 13-10. Skull of Epicríonops pmax
petersi. A. Dorsal. B. Ventral. maxpal fen ovalis
C. Lateral. D. Mandible in lateral
view and E. medial view. Redrawn naslac dj Lcolumella
from Nussbaum (1977). Abbreviations: orbit—' u stapedial artery f
ext = externa!; f = foramen; fen =
fenestra; maxpal = maxillopalatine;
naslac d = nasolacrimal duct;
pmax = premaxilla; pter =
pterygoid; pterquad = r*" — *K»WBa -. >i¿**¿^^ \ ~*^»—ai¿»~.. . '...

pterygoquadrate; quad = quadrate;

retroart p = retroarticular process; retroart p
spmax = septomaxilla; sq =
squamosal.

igin, extends anteriorly from the occipital área to the an- pectoral girdle and, therefore, lack an opercularis muscle
terior palate. The bone forms a broad floor to the neu- extending between the auditory apparatus and the girdle
rocranium, uniting the posterior exoccipital and otic As summarized by Wever and Gans (1976), the broac
ossifications to the sphenethmoid anteriorly. Posteriorly footplate of the columella (= stapes) lies in the fenestra
the ossification is integrated completely with that of the ovalis of the otic capsule, to which it is bound by an
exoccipitals and auditory capsules in the adult. annular ligament. The distal stylus of the columella artic-
Auditory apparatus.—Although not strictly a part of úlales with the quadrate. The skin and muscles covering
the auditory capsule, the middle ear bones are associated the auditory apparatus constitute the receptive surface
laterally with this structure in the región of the fenestra for sound waves.
ovalis. In caecilians, the middle ear bones are represented Eye muscles.—The eye muscles of caecilians consist
by a single element, the columella or stapes, which is of the four recti and two oblique muscles as describec
present in all caecilians except Scolecomorphus (Brand, for salamanders. The m. retractor tentaculi, innervated
1956; E. Taylor, 1969b). The columella is a robust en- by C.N. VI (abducens), retracts the tentacle and is the
dochondral element composed of a spheroid footplate homologue of the m. retractor bulbi of other amphibians.
and a distal style that extends rostrad from the anterior According to Badenhorst (1978), the m. levator bulbi has
end of the footplate to articúlate with the quadrate (Figs. been lost in caecilians. This muscle is not homologous
13-9, 13-10). Apparently, an operculum is absentin cae- with the m. compressor glandulae orbitalis of caecilians.
cilians, although H. Marcus (1935) suggested that it has as had been assumed previously, because the two mus-
been incorporated into the stapedial footplate, as it is in cles are innervated by different branches of the trigémina!
plethodontid salamanders. However, it should be noted nerve.
that, insofar as is known, the columella ¡n caecilians forms Neck muse/es.—Derivativos of both dorsal and ven-
from a single center of ossification. tral trunk musculature insert on the posterior surface of
the skull in caecilians. The skull is bound tightly by liga-
Muscles Associated with the Neurocranium. In ments, and movement is restricted mostly to the dorso-
contrast to salamanders and anurans, caecilians lack a ventral plañe. Three pairs of muscles are derived from
 Musculoskeletal System
toe dorsal trunk musculatura—the mm. rectus capitís su- and are united posterodorsally with their shared medial 307
penor. intertransversarius capitis superior, and intertrans- wall (septum nasi) via a process known as the oblique
«ersarius capitis inferior. These muscles insert on either cartilage. Posteroventrally an oblique cartilage (infranarial
• oí the base of the skull above and below the occipital cartilage) unites the alary cartilage with the floor (solum
yles and are responsible for raising the head and a nasi) of the nasal capsule.
1 amount of lateral movement. Some additíonal lat- Norial muscles.—Bruner (1914) reported the occur-
: movement is affected by the m. longus capitis, which rence of a constrictor and dilatator muscle of the externa!
• ¿erived from the ventral trunk musculature and inserís nares of Siphonops. Although the presence of these mus-
• the craniovertebral joint. cles has not been documented in other taxa, it is likely
that they are present in order to cióse the nares when
I Capsule. Relaüve to other Recent amphibians, the organism burrows.
< nasal capsules of adult caecilians are structurally sim-
(Fig. 13-11). The lack of interna!, cartilaginous sup- Dermal Investing Bones and Braces. The numbers
probably is correlated with the extensive develop- and configurations of dermal invesüng and bracing ele-
nt of rostral dermal bones (i.e., nasals, premaxillae, ments among caecilians are highly variable (Figs. 13-9,
Tüxülopalatines, septomaxillae, and vomers). 13-10, 13-12), and the nomenclature of the elements is
Strucíure of nasal capsule.—The medial and posterior inconsistent. Ichthyophiid and rhinatrematid caecilians have
i of the nasal capsule are formed by the mesethmoid the greatest number of cranial elements.
pcrion of the sphenethmoid. The floor of the capsule is Dorsolateral componente.—Dorsally, the nasal cap-
rcrr.posed of lateral extensions from the mesethmoid, the sules and sphenethmoid are invested by three pairs of
atal processes of the maxillae and premaxillae, and the bones—the nasals are anterior and flanked posterolat-
•omers. The olfactory organs lying within the nasal cap- erally by the frontals (= lacrimáis of some authors); the
are supported internally by struts arising from the frontals lie posterior to the nasals. The posterior braincase
somers, septomaxillae, and maxillopalatínes in combina- is roofed by paired parietals. Among advanced caecilians,
ion with various cartilaginous structures. The anterior end the nasal and premaxilla are fused into a single bone, the
3 each nasal capsule is formed by a cup-shaped cartilage nasopremaxilla. Similarly, the prefrontal is incorporated
cartílago cupularis, or alary cartilage of anurans and sala- into the facial process of the maxillopalatine. The lateral
nders), which also supports the terminal nares. Anter- wall of the nasal capsule is composed of the septomaxilla
medially the alary cartilages rest against the premaxillae, (or the nasopremaxilla with which the septomaxilla is fused

A
pmax med ¡nf pnas p
ext naris
pmax
spmax
nasal
vomer
orefrontal maxpal
^ je lamina orbitonasalis choana
aostfrontal
: :al Vf sphenethmoid

quad
ad

Figure 13-11. Skull of Ichthyophis glutinosas with dermal bones removed from right side to show
underlying chondrocranial elements; bones are stippled and cartilaginous structure shown in gray.
A. Dorsal. B. Ventral. Redrawn from a graphic reconstruction by M. Visser (1963). Abbreviations: c =
cartilage; ext naris = externa! naris; maxpal = maxillopalatine; med inf pnas c = medial inferior prenasal
cartilage; pmax = premaxilla; pter = pterygoid; pterquad = pterygoquadrate; quad = quadrate; spmax =
septomaxilla; sq = squamosal.
MORPHOLOGY
308 ¡n some caecilians) anteriorly and the facial process of sence of an orbit, the relationship of the tentacular and
the maxillopalatine. The tentacular foramen or groove orbital openings, and the configuration of bone sur-
lies in this facial process. The association of the posterior rounding the orbit (Fig. 13-13). In species oí Ichthyophis
margin of the facial process of the maxillopalatine with and Uraeotyphlus there is a discrete orbital (= ocular or
other elements varíes depending on the presence or ab- postfrontal of some authors). This bone forms either the
entíre orbit except for a small portion of its ventral mar-
gin, or only the posterior half of the orbit; portions of the
orbit not formed by a circumorbital bone are formed bv
the facial process of the maxillopalatine, which forms the
subocular facial bone that articúlales posteriorly with the
squamosal. Most caecilians lack a discrete circumorbit¿
element; the component may be lost entirely, or it mz'.
have fused posteriorly with the squamosal or ventrally
with the maxilla. Thus, in most species the margin of the
orbit is formed by the maxillopalatine anteriorly and an-
teroventrally and the squamosal dorsally and posteriorly.
In some caecilians (e.g., Epicrionops petersi and species
of Caecilia), the entíre orbit lies within the facial process
of the maxillopalatine.
The squamosal is a broad, posterolateral investing bone
of the temporal región. In most caecilians, which are ste-
gokrotaphic as adults, the bone articúlales dorsally with
the frontals and parietals (Fig. 13-9). In species that are
slightly zygokrotaphic, the squamosal has an incomplete
articulation with both roofing elements (Fig. 13-10). The
more marked the zygokrotaphy, the greater the témpora!
opening between the squamosal and the cranial roofing
bones. Absence of an articulation of the squamosal with
the parietal seems to be more common than absence of
an articulation with the frontal (Fig. 13-12). In extreme
zygokrotaphy (e.g., Epicrionops petersi), the squamosai
lacks any articulation with dermal roofing bones and in-
stead forms an arch between its remaining artículations
with the auditory capsule and quadrate posteriorly and
the facial process of the maxillopalatine anteriorly (Fig.
13-10).
Ventrolateral components.—In all caecilians, the
maxilla is fused to the palatine to form the maxillopala-
tine, a multifunctional bone (Figs. 13-9, 13-10). The fa-
cial process of this bone is a lateral covering bone for the
cheek, and the dental ridge serves as a primary element
of the upper jaw. The palatíne portion is a ventral, shelf-
like element that forms the lateral and posterolateral por-
tion of the palate, bears a row of teeth, and braces the
upper jaw via medial articulaüons with the vomer and
sphenethmoid and a posterolateral articulation with the
ectopterygoid (if present as a sepárate element), ptery-
goid, or pterygoquadrate. Similarly, the premaxilla (or
nasopremaxilla, if the premaxilla is fused with the nasal)
serves several functions. Its rostral portion supports the
anterior end of the nasal capsule, whereas its dental ridge
completes the maxillary arcade of the upper jaw. The
Figure 13-12. Dorsal views of caecilian skulls redrawn from palatine shelf of the premaxilla forms the anterior end of
photographs in E. Taylor (1969) showing a uariety of skull shapes
and dispositions of cranial roofing bones. B—F are examples of
the palate, articulating with the palatine posterolaterally
stegokrotaphic species of the family Caecilüdae, whereas A is a and the vomer posteriorly.
zygokrotaphic representative of the family Ichthyophiidae. Ventral components.—The central elements of the
A. Ichthyophis kohtaoensis. B. Caecilia nigricans. C. Hypogeophis
rostratus. D. Oscaecillia ochrocephala. E. Afrocaecilia uluqurensis. caecilian palate are the paired vomers (= prevomers of
F. Idiocranium russeli. some authors). These dermal elements underlie the nasal
 Musculoskeletal System
and sphenethmoid, bear an inner row of teeth quadrate and a long retroarticular processs that serves as 309
us with those of the maxillopalaünes, and, to- an attachment site for three major jaw muscles.
th these latter elements, form the margins of the Dentition.—All jaw bones bear teeth in caecilians. In
nac. The extent of the medial articulation of the addition, there is an inner, palatal series on the vomer
is variable. Apparently the anterior ends of the and the palatine portion of the maxillopalatine. Because
articúlate with one another in nearly all species. of the relative positions of the upper and lower jaws, the
ver. in many taxa the medial margins diverge pos- mandibular teeth fit between the two rows of upper teeth.
• : m one another to articúlate with the dagger- Caecilian teeth are pedicellate and generally recurved
•E ruJmform process of the parasphenoid medially. Al- (Fig. 15-20B). The shape of the crown, while consistent
:~ :.".e parasphenoid is considered to be an integral within a species, is highly variable among species
•^r :: :r.e os básale (i.e., posterior braincase) in caeci- (M. Wake and Wurst, 1979). The cusp may be mono-
•; interior half clearly is also a major componen! cuspid or bicuspid, recurved or subconical, and may bear
; r;!ate. lateral flanges of varying degrees of development. Re-
r some caecilians (e.g., species of Grandisonia, Schis- placement teeth develop interior to the older rows of
wnezopum, Herpe/e, Geotrypetes, Siphonops, Gym- teeth in an altérnate sequence; as older crowns are lost
?- í 3-called ectopterygoid has been identified (Fig. and pedicels resorbed, the younger teeth move periph-
3-10). This bone ( = pterygoid of some authors) braces erally to replace them (M. Wake, 1976, 1980d).
;:ei ior palatal portion of the maxillopalatine against
; vjoid ( = pterygoid process of the quadrate of Suspensorium. The suspensión and bracing of the
íosx authors). jaws in caecilians is a highly integrated, robust mecha-
nism that differs from the suspensory apparatus of sala-
"-oper and Lower Jaws. The upper jaw of caecilians manders and anurans in the pattern of masticatory mus-
s romposed of the premaxilla (or nasopremaxilla if fusión cles and in the involvement of the columella (= stapes)
has occurred) anteriorly and the maxillopalatine poste- in the mechanism.
scry (Figs. 13-9, 13-10). The mandible consists of two Skeletal componente.—The central suspensory ele-
taoadly overlapping dermal elements, the pseudodentary ment is the pterygoquadrate (so named because the pter-
ir.c pseudoangular, which are attached to each other by ygoid arises as a flange from the quadrate). The quadrate
Srrous connective tissue and, in a few species, a remnant ( = palatoquadrate of salamanders) portion of mis bone
rr Meckel's cartilage. As described by Bemis et al. (1983), articúlales with the neurocranium and, distally, the pseu-
•fx mandibular symphysis is a butt joint. The pseudoan- doangular of the mandible; it also articúlales posteriorly
aLar bears a U-shaped facet which articúlales with the with the columella and is overlain by the squamosal. The

Figure 13-13. Lateral views of caecilian skulls

redrawn from photographs in E. Taylor (1969).
Teeth are shown only if they were present in the
specimen. A. Ichthyophis beddomei
(Ichthyophiidae). B. Ichthyophis kohtooensis.
C. Caudacaecilia larutensis (Ichthyophiidae).
D. Siphonops annulatus. (Caeciliidae).
E. Idiocranium russeli (Caeciliidae).
F. Gegeneophis ramaswamii (Caeciliidae).
G. Geotrypetes seraphini (Caeciliidae). In
A—C note presence of sepárate premaxillae,
septnmaxillae, and prefrontals. A and B have
sepárate orbital bones. D—F ¡Ilústrate fusión of
rostral bones and variation in the development
of the facial process of the maxillopalatine and
its association with the orbit and/or tentacular
opening.
MORPHOLOGY
latter bone artículates to varying degrees with the frontal is some evidence that the levator mandibulae extern-¿
and parietal dorsally, and anteriorly is attached firmly to also acts to cióse and protract the lower jaw. The thin
the maxillopalatíne; thus, the squamosal serves as a cheek muscle in this series is the m. levator mandibulae pos-
bone as well as completing the maxillary arcade and serv- terior, which originales on the ventromedial surface :r
ing as a suspensory element. The pterygoid portion of the quadrate and exits the skull through the subtempora
the quadrate provides an internal strut between the pos- fenestra to insert on the ventromedial surface of the re-
terior end of the maxillopalatíne and the lower end of troarticular process of the mandible. The fourth interna
the quadrate. If an ectopterygoid is present, it lies be- levator is the m. levator quadrati, a straight, paralle;-:-
tween the pterygoid flange and the maxillopalatine. bered muscle that extends from the wall of the neurc-
Suspensory muse/es.—The masticatory musculature cranium to the pterygoid process of the quadrate. Ths
of caecilians has been reviewed most recently by Bemis muscle may act to restrict downward rotatíon of the
et al. (1983) and Nussbaum (1983). As one would sus- quadrate during periods of contracüon of the other three
pect from the configuratíon of the skull in this group, the levators. There is no known homologue of the m. levator
pattern of the levator and depressor muscles is quite dif- quadrati in salamanders or anurans.
ferent from that of salamanders and anurans. On the In caecilians the m. interhyoideus has assumed a total',
basis of their study of Dermophis mexicanas, Bemis et different function than in salamanders and anurans. Ir-
al. subdivided the levator muscles into two groups—in- stead of being a member of the mandibular musculaturt
ternal and lateral. The four internal levators arise from it is a levator of the jaw in caecilians. The muscle anses
the lateral wall of the braincase, the inner surface of the from the fascia of the ventral and lateral surfaces of r>£
dermatocranium (primarily from the squamosal), and the body and inserís by means of a tendón on the ventra.
pterygoquadrate (Fig. 9-2). The m. levator mandibulae surface of the retroarticular process of the mandible. TSí
anterior filis most of the dorsal portion of the adductor muscle is single in some caecilians but may be separa:?:
cavity. Posterior to the latter muscle is the m. levator into anterior and posterior components in others (Nuss-
mandibulae externus. Both of these muscles function as baum, 1983). The m. interhyoideus (or m. interhyoide-S
a unit to raise the lower jaw on which they insert. There posterior in those caecilians with anterior and posterior

Cb

Figure 13-14. Hyobranchial skeletons of caecilians in ventral view redrawn from Nussbaum (1977).
A. Epicrionops (Rhinatrematidae). B. Rhinatrema (Rhinatrematidae). C. Ichthyophis (Ichthyophiidae).
D. Gymnop/s (Caeciliidae). E. Typhlonectes (Typhlonectidae). F. Sco/ecomorphus (Scolecomorphidae).
Abbreviations: ar = arytenoid cartilages; Bb 1 = Basibranchial I; Cb I—IV = Ceratobranchials I—IV;
Ch = ceratohyal.
 Musculoskeletal System
corr.ponents) pulís the retroarticular process back and Skeletal componente.—The hyoid of most caecilians 311
aDUTi. thereby causing the jaw to rotate upward from an consists of a series of fíat, cartilaginous, recurved ele-
cpcn positíon. It is the major muscle of jaw elevation in ments to which muscles attach in the guiar región (Figs.
eaecilians, and, so far as is known, its function in this 9-2, 13-14). The most anterior elements, the ceratohyals

f
yaup is unique among tetrapods. and first pair of ceratobranchials (I) are united midven-
The m. depressor mandibulae is a massive muscle that trally by Basibranchial I, occasionally termed the copula.
minates on the posterolateral surface of the skull. Fibers Posterior to this unit is Ceratobranchial II which some-
o£ the fan-shaped muscle converge ventrally to inserí on times bears a small, anteromedial extensión that repre-
±K dorsal surface of the retroarticular process. Contrac- sents the remnants of Basibranchial II. Ceratobranchi-
4or. of this muscle pulís the process forward and up, als III-V are fused posteriorly into a single, broad ele-
racsing the jaw to rotate downward from a closed posi- ment. The larynx lies within the are of this posterior ele-
ment.
Mandibular and hyoid muscles.—The principal mus-
Hyobranchial Apparatus. The hyoids of adult cae- cles used in swallowing are the mm. dilatator laryngis,
sians are relatively unchanged from the larval condition two groups of constrictors, and the m. intermandibularis.
sr.d much less specialized than those of most salaman- The m. cephalodorsosubpharyngeus of salamanders and
TS and anurans. This doubtless is associated with the the levator bulbi of salamanders and anurans are not
use of the tongue in feeding by caecilians. present.

vomer

palatme

cr par (pro)
exoc—i

spheth—i fpar

nasal
sq

palatme columella
exoc
pter
pmax
max
prsph —1

¿
mmk mmk
-angspl-
-dentary-
Figure 13-15. Skull of Gastrotheca walkerí. A. Dorsal. B. Ventral. C. Lateral. D. Mandible in lateral view.
E. Mandible in medial view. Abbreviations: alary p = alary process; anglspl = angulosplenial; cr par =
crista parotica; exoc = exoccipital; fpar = frontoparietal; max = maxilla; mmk = mentomeckelian bone;
occ con = occipital condyle; pmax = premaxilla; pro = prootic; prsph = parasphenoid; pter = pterygoid;
qj = quadratojugal; spheth = sphenethmoid; sq = squamosal.
MORPHOLOGY
312 Mm. interhyoideus and dilatator laryngis cervicis is a forward continuation of the posterior ventra.
If single, the m. interhyoideus posterior acts to cióse trunk musculature (m. rectus abdominis) that inserts
the lower jaw rather than to elévate the hyobranchial the posterior ceratobranchials. The latter muscle has
apparatus. In most caecilians, which have a m. inter- serial connecüon with the strap-like m. geniohyoic
hyoideus anterior, the latter muscle elévales the hyo- that inserts on thr first ceratobranchial and arises frccr
branchial apparatus, whereas the m. interhyoideus pos- the anterior margin of the mandible. Contraction of rhese
terior adducts the jaw. The laryngeal muscle complex acts muscles retracts and protracts the hyoid, but does rae.
to open and cióse the glottis. The m. dilatator laryngis depress the jaw as it does in other amphibians. The ai
arises from the fused third and fourth ceratobranchials levator arcus branchiales (not present in metamorphoser
and inserís on the laryngeal cartílage. Most caecilians have salamanders or anurans) has a fan-shaped origin frca
two sets of constrictors, one that inserís on the arytenoid the dorsal fascia of the trunk musculature. The muscas
cartilage anterior to the insertion of the m. dilatator lar- passes ventral, deep to the m. interhyoideus, and insers
yngis and a second set that inserts posterior to this mus- onto the hyoid, which it elevates. Two deep visceral mus-
cle. The anterior set of constrictors is absent in Siphonops cles that may act to move the hyoid are the mm. trans-
(Edgeworth, 1935). The m. intermandibularis is repre- versalis ventralis i and iv which extend between the hyoc
sented by a thin, superficial sheet of transverse muscle and a median raphe that underlies the tráchea.
fibers that origínate along the medial edge of each man-
dible and insert on a narrow, medial raphe. Contracflon M. genioglossus
of this muscle elevates the hyoid and buccal floor. Apparently the tongues of caecilians are composed soie?.
of the m. genioglossus; the hyoglossus of salamancas
Mm. rectas cervicis, geniohyoideus, levator and anurans seems to be absent.
arcas branchialis, and transversalis i and iv
Muscles involved in the movement of the hyoid and Anurans
the limited movement of the tongue are the mm. rectus In comparison to salamanders and caecilians, there ¿ í
cervicis, geniohyoideus, levator arcus branchiales, and great deal more literature on anuran cranial osteology. =
transversalis ventralis i and iv (Fig. 9-2). The m. rectus summary of which appears in Trueb (1973). The appar-

mferior prenasal c
• crista subnasalis
pmax superior prenasal c

tect nasi alary c solum nasi

vomer
obligue c ant max p choana
nasal pl termínale — palatine
max pl antorbitale
sphenethmoid
pter p
tect trans
tect med

quad-
quad crista parotica basal p-1
pter parietal fen
prootic—' tect synoticum
Figure 13-16. Skull of Rana escalenta with dermal bones removed from right side to show underlying
chondrocranial elements; bones are stippled and cartilaginous structures are shown in gray. A. Dorsal.
B. Ventral. Redrawn from Gaupp (1896). Abbreviations: ant = anterior; c = cartilage; fen = fenestra;
fpar = frontoparietal; max = maxilla; p = process; pl = planum; pmax = premaxilla; prsph =
parasphenoid; pter = pterygoid; qj = quadratojugal; quad = quadrate; sq = squamosal; tect = tectum;
tect med = tectum medialis; tect trans = tectum transversalis.
 Musculoskeletal System
: rchness of this resource is deceptive because of the may be limited to the anterior part of the orbit, just be- 313
: r.umber of species of anurans (more than 3400 as hind the nasal capsules. In the majority of taxa (e.g.,
íed to 350 of salamanders and 160 of caecilians) Rana, Bufo, Hyla), the sphenethmoid is ossified ante-
~e anatomical diversity of anurans. Trueb (1973) riorly to form the posteromedial wall of the nasal capsule,
a synthesis of the major evolutionary trends in and to encircle completely the anterior part of the brain
osteology. Synonyms for the ñames of various throughout the orbital región. In a few hyperossified taxa
¡ and an extensive list of the literature are provided (e.g., pipids, Brachycephalus), ossification of this element
: paper. The terminology used in the following ac- may invade cartilage separating the orbit from the nasal
i follows that of Trueb except where noted. Read- capsule, and the bone may be fused with adjacent dermal
i «-shing more detailed descriptions of internal features investing elements such as the nasals, frontoparietals, and
t±£ anuran skull should consult Trueb (1968, 1970a) parasphenoid.
references cited therein. The prootic lies posterior to the sphenethmoid. In most
Because of the diversity of cranial architectural types anurans its anterior margin forms the posterior edge of
erizing anurans, it is difficult to make generaliza- the optic foramen. Posterolateral ossification of the prootic
• about them relative to caecilians and salamanders. gives rise to the auditory capsules. Like the spheneth-
the skulls of anurans are broad and fenestrate moid, the prootic always bears a large dorsal fenestra
13-15, 13-17, 13-18). The number of cranial ele- that is contiguous with that of the sphenethmoid. In most
is reduced relative to other amphibians, and the anurans, the ossified portions of the prootic are united
••pensorium (i.e., jaw artículation) usually is located to- medially, and posteriorly are fused indistinguishably with
the posterior limit of the skull. Those parts of the the exoccipitals to form one massive element that houses
'. T.volved with sensory systems (e.g., olfaction, hear- the posterior end of the brain and the otic organs; this
:end to be much more elabórate than those of sal- element has been referred to as the otoccipital by some
ers and caecilians. The palate is poorly developed, authors. In hypo-ossified anurans, ossification of the prootic
: dentition is ;educed. may be limited to the anterior wall of the auditory capsule
; "... of the same general works cited for the cephalic and to the posterior área of the orbit (e.g., Notaden), in
ature of salamanders also apply to anurans. The which case fusión with the exoccipital does not occur.
exhaustive summary exclusive to anurans is that of The posterior end of the neurocranium is formed by
(1896) on the anatomy of Rana escu/enta. Al- the exoccipitals that flank the foramen magnum and form
the summary is detailed, in many cases it is dif- the occipital condyles. The exoccipitals sometimes fuse
to reconcile myological homologies between anu- with one another dorsally and ventrally and with the
; and salamanders because Gaupp frequently applied prootics anteriorly to complete the auditory capsule.
; derived from the study of human anatomy to the Auditory apparatus.—Most anurans possess a com-
Jes of anurans. General descriptions of cephalic plete auditory apparatus composed of a plectrum and an
snusculature are available for Rheobatrachus silus operculum (Fig. 4-11). The operculum is a small, carti-
V Davies and T. C. Burton, 1982), Phrynomantis stic- laginous element that lies in the posterior portion of the
xnaster and other microhylids (T. C. Burton, 1983a, fenestra ovalis—a lateral opening in the auditory capsule.
t983b); these are among the most complete descriptions The plectrum lies anterior to the operculum and consists
srce that of Gaupp. of an expanded, ossified footplate and an ossified stylus
(together called the columella or stapes), and distal car-
rocranium. The braincase of anurans can be tilaginous elements. The footplate filis the anterior portion
T.ought of as a T-shaped box (Fig. 13-16). The leg of of the fenestra ovalis, and the columellar stylus extends
fie T extends posteriorly from the nasal región to the anterolaterally from the auditory capsule toward the side
auditory región, and the auditory capsules form the head of the head. The distal end of the stylus bears cartilagi-
rt ±e T. The neurocranium is composed of only five nous elements that are synchondrotically united with the
bones—the sphenethmoid, and the paired prootics and tympanic ring, which lies beneath the skin on the side of
cxDccipitals. In the orbital and preorbital regions, the the head and supports the tympanic membrane that is
srr.enethmoid forms the braincase and contributes to the visible externally. In many anurans, the sound-conduct-
—«dial and posterior walls of the nasal capsule. Its pos- ing apparatus is reduced (e.g., Telmatobius) or lost (e.g.,
jeror limit lies at the level of the optic foramen, the an- Rhinophrynus). Frequently, the tympanum, tympanic
terior margin of which is formed by the sphenethmoid. annulus, and the entire plectrum are lost, leaving only
The sphenethmoid always has a large dorsal fenestra that the operculum in the fenestra ovalis (e.g., Rhinophry-
s covered to varying degrees by dermal investing bones nus). Insofar as is known, the operculum always is re-
rigs. 13-17, 13-18). Ossification of this endochondral tained; however, in pipid frogs, the operculum may be
¿ement is highly variable among anurans. Among poorly incorporated into the footplate of the columella (de Vil-
3ssified species (e.g., Ascaphus, Notaden, and some mi- liers, 1932).
crohylids), the two halves of the sphenethmoid fail to Muse/es of the auditory región.—Most anurans, like
_nite in bone dorso- and ventromedially, and ossification salamanders, have muscles that origínate from the pec-
MORPHOLOGY
314

Figure 13-17. Dorsal (left) and ventral (right) views of anuran skulls. A. Barbourula busuquanensis
(Discoglossidae). B. Rhinophryus dorsalis (Rhonophyrnidae). C. Pelobates fuscus (Pelobatidae). D. Notaden
nichollsi (Myobatrachidae). E. Leptodacfylus bolivianus (Leptodactylidae). F. Caudiverbera caudiverbera
(Leptodactylidae). G. Brachjicep/io/us ephippium (Brachycephalidae). H. Rhamphophyrne festae
(Bufonidae).
 Musculoskeletal System
315

Bjnre 13-18. Dorsal (left) and ventral (right) views of skulls of hylid frogs. A. Gastrotheca ovifera.
B. Pseudacris clarkii. C. Phyllomedusa venusta. D. Hemiphractus proboscideus. E. Smiíisca baudinii.
F. Phrynohyas uenulosa. G. Triprion petasatus. H. Osteocephalus /eprieurii.
MORPHOLOGY
toral girdle and insert on the opercular-plectral apparatus. 1896) extends from the neural arch of the first ver
The so-called m. opercularis of anurans seems to be ho- anteriorly to the occiput in the región of the for
mologous with the muscle of the same ñame in sala- magnum.
manders that is derived from the m. levator scapulae. As
depicted by Wever (1979, Fig. 1), the m. opercularis is Nasal Capsule Of the Recent amphibians, anura«
the most dorsal of a series of three muscles; it arises from probably have the most complex nasal capsules. Tne
the anteromedial, ventral surface of the suprascapula and nasal organ consists of a complicated series of nasal sa3
inserts on the operculum in all anurans examined thus and ducts that, in the absence of a well-developed pa¿at
far except the pipids, which lack a discrete operculum and rostral roof, are supported internally by the sepr-
(Fig. 4-11). The muscle was shown by Becker and Lom- maxillae and a variety of cartilages.
bard (1977) to have distinctive flbers that are small. The Structure of nasal capsules.—The capsules lie arvE-
m. columellaris is inferior to the m. opercularis; it arises rior to the sphenethmoid within the área enclosed by ne
on the suprascapula posterolateral to the opercularis and premaxillae and maxillae (Fig. 13-19). These latter ee-
inserts by means of a ligament to an extended process ments, along with the nasals and vomers ( = prevorres
of the footplate of the columella (Fig. 4-11). The deri- of Trueb, 1973, and other authors), provide support =nr
vation of this muscle is not known, although it would protection for an intricate system of nasal cartilages. ~
seem reasonable that it might have been derived from anterior and anterolateral walls of the nasal capsule 20*
the m. levator scapulae also; it has no homologue in formed by the cup-shaped alary cartilage that suppr<rs
salamanders. The m. levator scapulae lies beneath the the anterolateral margin of the externa! naris. A smal roe
auditory muscles; it originales from the medial surface of of cartilage (the superior prenasal cartilage) extends frrcí
the suprascapula and inserts on the sides of the nasal the alary cartilage anteriorly to abut the posterior face a
capsule. Functionally, it is not a cephalic muscle and the premaxilla. The floor (solum nasi), roof (tectum naái.
therefore will be dealt with in the section: Appendicular and the medial wall (septum nasi) separating the naal
Skeleton. The actions of the opercular and columellar capsules are formed in sphenethmoidal cartilage and mas.
muscles are discussed in Chapter 4. be ossified to varying extents. The only other bony áe-
Eye muscles.—The eye muscles of anurans are the ments infernal to the nasal capsule are the septomaxiae.
same as those described for salamanders. a pair of bones present in all anurans. The septomaxi*
Necfc muse/es.—The skulls of anurans, like those of is dermal in origin but lies imbedded in cartilage meda.
salamanders, are attached to the vertebral column by to the maxilla and supports the anterior end of the r*-
derivatives of the dorsal trunk musculature, specifically solacrimal duct which extends from the nasal organ pos-
the mm. intertransversarii capitis superior and inferior. teriorly to the región of the eye. The posterolateral a~c
The anterior interspinalis ( = m. intercrurales of Gaupp, posterior walls of the nasal capsule are formed by r*.n

qj
pter
max frontoparietal
Figure 13-19. Isometric view of
anterior cranium of Rhinophyrnus
dorsalis to show cartilaginous
components of nasal capsule and
their relationships to overlying bones.
Cartilage is shown in gray, the spmax pía term
septomaxillae are stippled in black, ext nar
and the positions of the maxillary pía ant
arch and dermal investing bones are
al c
indicated by outlines. Abbreviations: tect ñas
al c = alary cartilage; al proc vom
pmax = alary process of premaxilla; pter prcc
ant max proc = anterior maxillary sup pnas c
process; c obl = oblique cartilage;
corn trab = cornu trabeculae; cr inf pnas c
sub = crista subnasalis; ext nar =
external naris; inf pnas c = inferior sept ñas
prenasal cartilage; max = maxilla; pmax
pía ant = planum antorbitale; pía
term = planum termínale; pmax =
premaxilla; pter = pterygoid; pter
proc = pterygoid process; qj =
quadratojugal; sept ñas = septum
nasi; spmax = septomaxilla; sup al proc pmax—' ant max proc
pnas c = superior prenasal cartilage; cr sub corn trab
tect ñas = tectum nasi; vom = 5mm
vomer. Reproduced from Trueb and lam inf
Cannatella (1982).
 Musculoskeletal System
lous walls, the planum termínale and planum toparietal fenestra (the dorsal neurocranial fenestra formed 317
de, respectively. There is a variety of other in- in the sphenethmoid and prootíc) in the orbital región
I cartilaginous struts and braces associated with the (e.g., centrolenids). In most anurans, the frontoparietals
sa. capsule. Details about these structures are available are larger elements that cover at least the posterior part
Trueb (1968, 1970a) and Jurgens (1971) and refer- of the fenestra and the medial área of the prootics in the
; in those publications. auditory región. Frequently the medial margins of the
.Soria/ muscles.—The occurrence of narial muscles in frontoparietals articúlate with one another throughout their
. • í ¡5 a matter of dispute that was reviewed most lengths (e.g., Rana, Bufo) to roof the neurocranium com-
•cer.ry by Gans and Pyles (1983). According to these pletely. Depending on the degree of hyperossification,
- - '.vho examined more than 40 species of anurans, the frontoparietal may be elaborated to produce a su-
• • . . muscle is absent in the narial región. Although a praorbital flange over the orbit and/or a temporal flange
::h muscle (m. lateralis narium) may be present in that extends posterolaterally over the otic capsule toward
aa-€ taxa (e.g., Rana), it is not present in all (e.g., Hy/a the side of the skull. In some anurans (e.g., pipoids and
£ - if present, smooth muscle could not be involved Pelobates) the frontoparietal is azygous (i.e., single),
: -al closure. completely covers the sphenethmoid, and overlaps the
Ecgeworth (1935) reported the presence of a smooth posterior margins of the nasals (Fig. 13-17).
. m. labialis superior) along the upper lip in Three additional dermal roofing elements are present
in a few species. Among hyperossified, casque-headed
anurans (e.g., Triprion and some Gastrotheca) there fre-
Pejmal Investing Bones and Braces. Relative to quently is a dermal sphenethmoid that lies above the
so— salamanders and caecilians, most anurans have fen- sphenethmoid between the nasals and frontoparietals (Fig.
«srate skulls with open temporal regions (i. e., gymno- 13-18). One peculiar, burrowing, casque-headed hylid
jctxaphic) which afford only minimal protection to the (Pternohyh fodiens) has an internasal element protecting
::anium and nasal capsules. As might be antici- the median part of the rostrum in front of the nasals.
. the number of dermal investing and bracing ele- Finally, the primitive discoglossid Bombina oríentalis has
has been reduced. Lacrimáis, pre- and postfron- an interfrontal bone that lies above the frontoparietal fe-
ais. and sepárate parietals are absent. The usual nestra medially between the anterior ends of the fron-
complement of dorsal roofing bones consists only of paired toparietals.
casáis and frontoparietals. A squamosal bone always in- Ventral componente.—Anurans usually have three
wests the lateral part of the suspensorium, and a paras- ventral investing bones—paired vomers anteriorly and a
phenoid and paired pterygoids invariably are present single parasphenoid posteriorly (Figs. 13-15, 13-17,
ventrally. Vomers and palatines may be reduced or ab- 13-18). Vomers frequently are absent (e.g., Pipa and
many other taxa), reduced, or undergo fusión in one of
Dorsal componente.—The paired nasals lie anterior two ways. The vomers may be reduced or fused medially
•E the ossified portion of the sphenethmoid (Figs. (some species of Xenopus), or fused with the palatines
13-15-13-18). They provide a dermal roof to the nasal to form a vomeropalatine (some microhylids). When
capsule, although the extent of protection afforded ob- present, the vomers form part of the palate and floor the
.-ously depends on the size of the nasals. Minimally, na- nasal capsules, and usually are associated with the pre-
sals are slim, diagonally oriented slivers of bone that cover maxillae and maxillae anteriorly and the sphenethmoid
only the posterior portions of the nasal capsules (e.g., posteriorly. They usually bear teeth on a dentigerous
-íScaphus and many small, arboreal hylids and centro- process or, occasionally, as in Hemiphractus, odontoids
jcnids). In many anurans, the nasals are more extensive (projections of bone resembling teeth).
zuadrangular elements that approximate one another The parasphenoid invests the braincase ventrally and
— edially, cover most of the nasal capsule, and bear a is present in all anurans. In most taxa, the bone is
posterolateral process (the maxillary process) that artic- T-shaped; thus, the posterolateral alae (wings) cover the
ulates with the maxillae to brace it against the neuro- auditory capsules laterally, and the anterior ramus (cul-
cranium. Obvious elaboratíon of the nasals occurs in two triform process) extends from the prootic región forward
groups of anurans— hyperossified, casque-headed spe- to termínate at the anterior margin of the orbital región.
cies (discussed separately) and some pipoid frogs. In the The single deviatíon from this plan is found among pipoid
case of the latter (e.g., Xenopus) the nasals fuse medially frogs in which the parasphenoid lacks posterolateral alae.
and grow downward to form part of the medial partition A few taxa (e.g., Pseudis paradoxa) bear odontoids on
septum nasi) between the olfactory organs. the parasphenoid. In hyperossified frogs (e.g., Brachy-
The second pair of dermal roofing bones lies posterior cephalus, Fig. 13-17G), the ossification of the para-
to the nasals; these are the frontoparietals that represen! sphenoid may be incorporated with that of the neuro-
the fusión of the frontal and parietal elements of other cranium.
amphibians. In their minimal configuration, the fronto- Of the two remaining pair of palatal elements—the
parietals are long, slender elements that flank the fron- palatines and pterygoids—the former frequently are re-
MORPHOLOGY
318 duced, lost, or fused (see discussion of vomer above), pium (about 16 mm snout-vent length, Fig. 13-17G) s
whereas the latter always are present. The palatine is ossified more heavily than a large Bufo marinus (aboír
absent in leiopelmatids, discoglossids, pipoids, and pos- 150 mm snout-vent length). Hyperossification can affec
sibly pelobatíds and pelodytids; in most other anurans it the structure of the skull in several ways. In the pipidí
is present as a slim, transverse element that braces the nearly all cartilaginous parís of the skull are replaced b>
upper jaw against the neurocranium. Reduction of the bone, and synostosis of dermal and endochondral ele-
palatine occurs in a medial to lateral direction so the ments tends to result in solid fusión of the braincase—
palatine always is associated with the maxilla laterally. the parasphenoid and frontoparietals are fused with the
True teeth never are present on the palatine, but the sphenethmoid and prootics. Hyperossification also car.
bone frequently bears a distinct ridge that may be serrate. affect the externa! dermal investing bones of the skull
The pterygoid is a triradiate element in all but two This development can be seen in most bufonids, mar.;,
genera of anurans. The bone basically has an inverted hylids (e.g., Aparasphenodon, Corythomantis, Gastro-
Y shape. The anterior leg of the Y articúlales with the theca, Hemiphmctus, Ptemohyla, and Triprion, Figs
maxilla, and the two posterior arms articúlate laterally 13-17, 13-18), and some pelobatids, leptodactylids (e.g..
with the quadrate of the suspensorium and medially with Caudiverbera, Fig. 13-17F), and ranids (Ceratobatra-
the auditory capsule, respectively. The pterygoid acts as chus), among others. In most anurans the first sign c:
a brace between the suspensorium and upper jaw and hyperossification is the appearance of sculptured pattems
the neurocranium. In several species, the pterygoid does on the surfaces of the dermal bones, a condition termec
not serve as a medial brace because its medial arm is exostosis. In its most generalized state, exostosis is ex-
reduced so that it does not articúlate with the auditory pressed as a poorly organized reticulate pattern. This
capsule, and in one taxon (Rhinophrynus, Fig. 13-17B) generalized pattern may be retained in the adult (e.g-.
it is absent. In Hymenochirus, the anterior arm of the Bufo) or may undergo modification during developmer.:
pterygoid is absent and along with other pipids, the pos- to produce intricate patterns of radial ridges such as those
terior arms of the pterygoid are expanded greatly to form found in the hylid Triprion petasatus. Further hyperos-
a píate that covers the otic capsule ventrally. sification is expressed by the hypertrophy of dermal ele-
Lateral components.—Paired squamosal bones that ments to increase their overall size and produce extensive
invest the quadrates laterally and articúlate medially with marginal flanges. In extreme examples (e.g., Triprion.
the crista parotica of the auditory capsule are present in Ceratobatrachus), the gymnokrotaphy of the basic ski£
all anurans, although the elements vary considerably in is disguised because only the orbital región of the skul
their degree of development. Among hypo-ossified anu- remains open. The most extreme expression of hyper-
rans (e.g., Notaden, Fig. 13-17D), the squamosal may ossification involves co-ossification of the dermal bones
be reduced to a sliver of bone applied laterally to the with the overlying skin. Bone forms in the dermis of the
quadrate. In most anurans, the squamosal is triradiate, skin during development and then fuses with the under-
bearing a ventral arm along the quadrate perpendicular lying cranial bone so that in the adult the skin is unitec
to the maxilla and two dorsal arms oriented horizontally completely to the bone below. This condition is typical
(Fig. 13-15). The posterior, or otic, ramus articulares with of many bufonids and hylids.
the prootic bone of the auditory capsule, thereby par-
ticipating in the suspensión of the jaws from the skull. Upper and Lower Jaws. The upper jaw of most anu-
The otic ramus frequently is expanded into an otic píate rans is composed of two or three pairs of bones— th¿
that overlaps the prootic. In hyperossified anurans (e.g., premaxillae, maxillae, and quadratojugals (Fig. 13-15
Triprion, Fig. 13-18G), the head of the otic ramus may The latter may be reduced or absent, but the former tv.-:
be elaborated to form a temporal arch that extends me- always are present.
dially to articúlate with the temporal flange of the ex- Premaxilla.—The paired premaxillae are located ar-
panded frontoparietal. Most anurans bear an anterior, or teromedially and syndesmotically united to one another
zygomatic, ramus on the squamosal that extends from medially and to the maxillae laterally. Typically, a pre-
the head of the squamosal toward the maxilla ventrally. maxilla is composed of three parts. The pars dentáis
In some taxa it articúlales with the maxilla, whereas in bears the dental ridge. A vertical strut, the alary process.
most it bears a ligamentous connection with the upper provides an abutment for supporting cartilages of the na-
jaw. In pipids, the squamosal has undergone a most sal capsule. A lingual shelf, the pars palatina, varies ir. rs
peculiar transformation. During development, ossification degree of development among anurans and serves as the
of this element is incorporated with ossification of the site for attachment of the soft tissue lining of the bucea
tympanic annulus, so that in adults the squamosal con- cavity. Generally, the premaxilla simply abuts the rnaxü
sists of a vertical element flanking the quadrate and an laterally, but in some taxa (e.g., some microhylids ar.c
anterior conch-shaped element that surrounds the distal Pe/tophryne) the maxilla overlaps the premaxilla latera^.
portion of the columella. Maxilla.—The maxilla bears the same three basic pars
Hyperossification.—Hyperossification is a phenome- as the premaxilla, although its vertical component is termec
non commonly observed among anurans. It is unrelated the pars facialis. The pars facialis forms the lateral wal
to size; thus, a species as small as Brachycephalus ephip- of the nasal capsule anterior to the orbit and may prov-:¿£
 Musculoskeletal System
5-pport to the upper jaw if the nasal articúlales with it. pends and braces the jaws against the skull in anurans is 319
Á'r.en present and complete, the quadratojugal com- the quadrate (= palatoquadrate of salamanders), which
petes the upper jaw posteriorly. The bone articulates usually is not visible in adults because it is covered by
i the maxilla anteriorly, and posteriorly it is integrated the ventral arm of the squamosal laterally and the lateral
the pars articularis of the quadrate. If reduced, the ramus of the pterygoid medially and posteromedially. The
r-adratojugal bears a ligamentous connection with the orientation of the quadrate coincides with that of the ven-
posterior end of the maxilla. tral arm of the squamosal; thus, in most anurans the long
One genus of hylid frog, Triprion, bears special men- axis of this cartilaginous element is more or less vertical
ren owing to its bizarre nature. The basic configuration and its upper end deflected slightly anteriorly. In histo-
:: :he upper jaw is like that of other anurans except that logical preparations, it is possible to see that the upper
-¿ maxillae bear broad, upturned lateral flanges that end of the quadrate is attached to the oüc capsule via a
articúlate with a single, large rostral element—the pre- small process, termed the oüc process. Basally, two other
-asal. This triangular, neomorphic dermal bone (Fig. cartilaginous processes provide support for the quadrate.
13-18G) lies anterior to the partes dentalis of the pre- The pterygoid process is invested by the pterygoid bone
—axillae. The alary processes of the premaxillae are ro- ventrally and then extends forward from the quadrate to
2ted forward so that they lie within the prenasal. Thus, fuse with a cartilaginous support of the maxilla which
T'iprion is the only frog known to have an addiüonal parallels and lies medial to this process. The pseudobasal
£€ment in its upper jaw. process extends posteromedially from the quadrate to
Dentition.—Maxillary and premaxillary denütion is articúlate with the anteroventral edge of the oüc capsule,
sporadic in occurrence. For example, all bufonids lack although this unión is fused in a few taxa (e.g., Bufo).
sjch dentition, but all hylids (except Allophryne) possess Leiopelmatids differ from all other anurans (for which
- When present, the teeth usually are spatulate and bi- data are available) in lacking a pseudobasal process. In
ruspid; however, in the pipid frog Xenopus, the teeth are this family, medial support of the quadrate is accom-
—.onocuspid, nonpedicellate, and fused to the maxillae modated by two processes—the basitrabecular and basal
sr.d premaxillae (Katow, 1979). In many carnivorous taxa processes—in much the same manner as in salamanders.
(eg., Ceratobatrachus, Hemiphractus, Xenopus, Cera- The basitrabecular process is produced from the basal
aophrysj, the teeth are modified to form fangs that may píate of the neurocranial floor and abuts the basal process
r-a recurved (Fig. 15-20C). Replacement teeth on all which arises as a medial outgrowth of the quadrate. Ven-
¿«enlate elements form interior to the older teeth in either tral support of these cartilaginous processes is provided
ar. altérnate or successive pattern. As older teeth are re- by the medial arm of the pterygoid. Although the quad-
sorbed, the younger teeth move peripherally to replace rate remains largely cartilaginous, perichondral ossifica-
nem (Gillette, 1955; C. Goin and Hester, 1961; Shaw, tion may occur along its medial margin, and the ventral
1979). end (pars articularis) that articulates with the mandible
Mandible.—The lower jaw of anurans is composed, usually is ossified. Ossification of the quadratojugal (if
—.aximally, of three pairs of elements (Fig. 13-15). Except present) is integrated with ossification of the pars articu-
r>. pipoids, a pair of mentomeckelian bones forms anter- laris. The three dermal investing bones involved with the
rmedially in Meckel's cartilage; the bones bear a syn- suspensorium (pterygoid, squamosal, and quadratojugal)
¿esmotic connection with one another medially. In pipids are discussed above with other investing and bracing ele-
and rhinophrynids the two halves of the jaw lack a sym- ments.
physis. The dentary invests Meckel's cartilage anterolat- Suspensory muse/es.—Anuran jaw musculature is a
erally and the angulosplenial invests the medial and pos- great deal more complex and variable than that of sala-
terior surfaces of Meckel's cartilage. Occasionally (e.g., manders, and has attracted considerable attention over
some microhylids) the dentaries articúlate anteromedi- the years with respect to its condition and its develop-
ally. The angulosplenial articulates with the quadrate pos- mental history. Sedra (1950) produced a monograph on
teriorly. Mandibular teeth are known to occur in only one the metamorphosis of the jaws and jaw muscles in Bufo
species of anuran, Amphignathodon guentherí, and these regularís, and de Jongh (1968) wrote on the functional
are borne on the dentary. In some other taxa (e.g., Ade- morphology of the musculoskeletal system in larval and
'.otus, Ceratobatrachus, Hemiphractus), the margin of the metamorphosing f?ana temporaria. Luther's (1914) study
dentary is modified to form toothlike serrations and an- of muscles innervated by the trigeminal nerve in am-
teriorly it bears a single large, fanglike odontoid. phibians is still one of the most complete accounts of
anuran jaw musculature, although it is based on only
Suspensorium. The anuran suspensory apparatus eight species representing six families. P. Starrett (1968)
usually is much less robust than that of either caecilians emphasized the variability of these muscles among anu-
or salamanders owing to the extreme gymnokrotaphy of rans in her discussion of the phylogenetic significance of
the skull. There is considerable variation in both the de- the jaw musculature. This variability has become increas-
velopment of the skeletal components and the nature of ingly apparent based on morphological studies such as
the associated musculature as elaborated below. that of Limeses (1965) on ceratophryine leptodactylids,
Skeletal components.—The central element that sus- M. Davies and T. C. Burlón (1982) on Rheobatrachus
MORPHOLOGY
320 m pter

m lev post long

m dep mand
m lev post mand sub
{¿¿yjj' m lev post mand ext C¡
m lev mand post artic-

D
m genhyd med
m genhyd lat
hyoid

m intermand
mandible

m interhyd- hyale
antlat p
postlat p
postmed p

m genglos bas
m genglos med

mandible

maxilla

tongue m omohyd

m hyoglos

Figure 13-20. Masticatory, mandibular, and hyoid musculature of representative anurans. A. Superficial adductor
muscles and B. deep adductor muscles of Rana temporaria, redrawn from Luther (1914). C. Superficial mandibular
musculature of Bufo marinus with medial raphe removed in upper right quadrant to expose deeper muscles.
D. Superficial (left) and deeper (right) hyoid musculature ofB. marinus. E. Tongue muscles of B. marinus. F. Deep hyoid
muscles ofB. marinus. Cartilage is stippled; raphes and membranes are hatched. Abbreviations: antlat p = anterolateral
process of hyoid; m dep mand = m. depressor mandibulae; m genglos bas = m. genioglossus basalis; m genglos med =
m. genioglossus medialis; m genhyd lat = m. geniohyoideus lateralis; m genhyd med = m. geniohyoideus medialis;
m hyoglos = m. hyoglossus: m. interhyd = m. interhyoideus; m intermand = m. intermandibularis; m lev mand post
artic = m. levator mandibulae posterior articularis; m lev post long = m. levator posterior longus; m lev post mand =
m. levator posterior mandibulae; m lev post mand sub = m. levator posterior mandibulae subexternus; m omohyd =
m. omohyoideus; m petrohyd = m. petrohyoideus; m pter = m. pterygoideus; m sternohyd = m. sternohyoideus;
m submen = m. submentalis; postlat p = posterolateral process of hyoid; postmed p = posteromedial process of hyoid.
 Musculoskeletal System

srus. and T. C. Burton (1983a, 1983b) on microhylids. (= m. temporalis of Gaupp, 1896), a member of the 321
~ne work that has been done is primarily descriptive, and posterior group of adductors. This muscle arises from a
—• date little is known about the functional correlates of median raphe on the skull roof, the lateral aspect of the
r.e variation. frontoparietal, and the dorsal and anterior surfaces of the
Anurans apparently have a basic complex of six ad- prooüc. Its fibers converge on a tendón that inserts on
ructor muscles (Fig. 13-20). Although they vary in rel- the medial margin of the angulosplenial. In some taxa, it
anve size and áreas of origin and insertion, these muscles is divided into superficial and deep layers. Another mem-
:an be divided into three topographic groups (Luther, ber of the posterior group is the m. levator mandibulae
1914)—an internal levator, two externa! levators, and posterior lateralis that arises from the ventral arm of the
tfiree or four posterior levators. The internal levator is the squamosal and inserts on Meckel's cartilage and the lat-
— levator mandibulae anterior longus ( = m. ptery- eral surface of the angulosplenial. The last of the posterior
goideus of Gaupp, 1896, and Luther, 1914). This muscle muscles is the m. levator mandibulae posterior articularis
generally arises from the dorsal surface of the skull roof which arises from the quadrate and inserts on the man-
»r.d from the lateral surface of the neurocranium, lies dible. The two remaining muscles belong to the external
anterior to the trigeminal nerve, and inserts via a tendón group. These are the m. levator mandibulae externus
en the medial margin of the angulosplenial of the man- which arises from the zygomatic process of the squamosal
dible. The m. levator mandibulae anterior longus may and inserts laterally on the mandible, and the m. levator
•x homologous with the m. levator mandibulae anterior mandibulae posterior subexternus which also arises from
::' salamanders, based on its forward position with re- the zygomatic ramus and inserts on the upper surface of
spect to the fifth cranial nerve. Posterior to this nerve lies the mandible. The homologies of these muscles with those
—e massive m. levator mandibulae posterior longus of salamanders are not certain.

Figure 13-21. Hyobranchial skeletons of anurans in ventral view. Bone is white and cartilaginous structure
are stippled. A. Leiopelma hochstetteri (Leiopelmatidae). B. Rhinophyrnus dorsaüs (Rhinophyrnidae).
C. Bombina varíegata (Discoglossidae). D. Leptodactulus ocellatus (Leptodactylidae). E. Heleioporus
albopunctatus (Myobatrachidae). F. Bu/o himalayanus (Bufonidae). Abbreviations: ant p hyale = anterior
process of hyale; antlat p = anterolateral process of hyoid píate; phyd = parahyoid bone; plat p =
posterolateral process of hyoid píate; pmed p = posteromedial process of hyoid píate.
MORPHOLOGY
322 The m. depressor mandibulae is a massive muscle that classic reference on variation in the anuran hyoid and :s
is composed of several slips, the number and origins of associated musculature. Tyler, in several papers (e.g..
which vary among species. The depressor is broad dor- 1971a, 1972), described variation in the superficial man-
sally at its origins which may include the dorsal fascia, dibular musculature and discussed its probable phylc-
the skull roof, otic región, and the squamosal. Ventrally, genetic significance within various groups of anurans
the fibers converge into a tendinous inserten at the pos- Magimel-Pelonnier (1924) described the tongues of marr.
terior end of the mandible. amphibians, especially anurans. Attenüon was focusec
on the functional aspects of this variation by Regal anc
Hyobranchial Apparatus. Anurans have the most Gans (1976), and the diversity and systematic signi±-
highly derived hyobranchial apparatus of any amphibians cance of the anuran tongue musculature was discussec
with the possible exception of plethodonüd salamanders. by Horton (1982b).
Moreover, there is marked variatíon in the structure of
this part of the musculoskeletal system; for the most part, Laryngeal and swallowing muscles
the significance of this variaüon is poorly understood. As in salamanders, the principal muscles used in swat-
Skeletal componente.—The anuran hyoid consists of lowing are the mm. dilatator laryngis, constrictoc
a central cartilaginous píate that has a shallow V-shape ( = sphincter) laryngis, intermandibularis, interhyoideus
in cross secüon (Figs. 4-3, 13-21). Two pair of attenuate, and levator bulbi. The m. dilatator laryngis (Figs. 4-3.
doubly recurved stmctures—the cornua or anterior hyale— 4-5), present in all anurans, originates from the poster-
arise from the anterolateral corners of the hyoid píate omedial process of the hyoid and inserís on the arylenoic
and curve posterodorsally above the píate to attach to cartílage. The constrictor or sphincter encircles the ary-
the ventral surface of the otic capsule. The cornua are tenoid cartilage (Figs. 4-3, 4-5). Usually it is sepárate:
missing in some anurans (e.g., pelodyüds) and discontin- into anterior and posterior parts, and from its origin cr
uous in some others (e.g., Rhinophrynus). The hyoid the hyoid píate inserís on a raphe. Many bufonids lac.-
píate usually bears three additional pairs of processes. íhe posíerior constrictor, and the muscle also ¡s absent ir.
Anteriorly on the píate, the anterolateral processes flank Bombina. In pipids íhe muscle is noí divided into anterior
the cornua laterally. Posteriorly, there are posterolateral and posíerior portions.
processes and a pair of long, bony posteromedial The mandibular musculature of anurans is especiad,
processes. The anterior cornua and posteromedial variable in íhaí many supplemenlal slips apparently have
processes are invariably present; however, the anterolat- arisen from the main muscle masses in various taxa (Ty-
eral and posterolateral pairs vary in both their presence ler, 1971a, 1972, 1974). The basic configuration of this
and shape. A few taxa (Rhinophrynus, Pelodytes, and sheet of muscles in anurans consists of íhe mm. sub-
leiopelmatids) have parahyoid bones associated with the mentalis, intermandibularis, and interhyoideus in an an-
central hyoid píate; these vary in number, posiüon, and terior to posterior sequence (Figs. 13-20, 13-22). The m
size, and their homologies, function, and histological deri- submentalis is a small bundle of short, íransverse fibers
vaüon are uncertain. The hyoid lies in the floor of the that unite íhe mandibular rami mosí anleriorly. Con trac -
mouth and serves as the site of insertion for a variety of tion of íhis muscle roíales fhe jaw symphysis by movinc
muscles associated with movement of the tongue and as the mentomeckelian bones. This action is linked to clos-
the origin of the m. hyoglossus which constitutes the main ing the external nares (Gans and Pyles, 1983) and is
body of the tongue. involved in íhe depression of íhe lower jaw in íhe initial
The laryngeal apparatus is derived from the larval slages of feeding. The m. intermandibularis consists of
hyobranchial skeleton, In most anurans, it is composed long, more or less íransverse fibers Ihal inserí on a mediad
of a pair of arytenoid cartilages that are supported by the aponeurosis and raphe, and unite the margins of íhe
cricoid ring (Figs. 4-3, 4-5). which is complete in most mandibular rami usually almosl to their posterior ends
species. It is incomplete dorsally in a few (e.g., peloba- Posterior to íhe m. iníermandibularis, and sometimes
tíds), ventrally incomplete in myobatrachids and soog- overlapping it, is the m. interhyoideus. The diversity of
lossids, and bears lateral gaps in at least one species of íhe size and structure of íhis muscle is associated with
Dendrobates. variation in íhe slructure of the vocal sac, which may be
Mandibular and hyobranchial muscles.—Since 1970, internal (Fig. 4-8) or exlemal, single and median (Fig. 4-
a great deal has been learned about the mandibular and 7), or paired lateral or posterolateral (see Chapter 4).
hyoid musculature of anurans, which is considerably more Depending on íhe disposition of íhe vocal sac, íhe mus-
complex and derived than that of salamanders. In anu- cles may lake the form of a relatively fíat sheet, or have
rans, the hyobranchial musculoskeletal system is involved a single, large posterior lobe or some degree of bilobate
in vocalization as well as ventilation and feeding, as the development. If the vocal sacs are internal and lateral,
majority of anurans feed by flipping the tongue anterior the m. interhyoideus is elaborated inlo a lubular exten-
to the snout (Gans and Gorniak, 1982a). The mecha- sión that lies posterolateral to íhe head. Obviously íhe
nisms of tongue protrusion in salamanders and anurans function of the m. interhyoideus in anurans is modified
is described in Chapter 9. Trewavas (1933) remains the from Ihal in salamanders.
 Musculoskeletal System
323

Distal tip of tongue

containing fibers of
Genioglossus medialis distalis

Hyoid (protruded)

Hyogtossus

Bmoglossus
medialis

Qenoglossus Mandible
basalis

Submentalis

Mandibular symphysis (depressed)

Figure 13-22. Cutaway of mandibular, hyoid, and tongue musculature of Bu/o marinus at the beginning of
: tongue-flip sequence. Bones are stippled, cartilage is white, and muscles are gray. Reproduced from Gans
and Gorniak (1982a) with permission of the AAAS.

Mm. geniohyoideus, omohyoideus, posteromedial process of the hyoid. The numbsr of pairs
and petrohyoidei of petrohyoids vanes. Some anurans possess four, whereas
Muscles that move the hyoid and tongue lie deep to others have only three, in which case the m. petrohyoi-
the mandibular series (Fig. 13-20). The most superficial deus iii is missing. Pipids have only one petrohyoid; the
of these is the strap-like m. geniohyoideus that arises identity of mis muscle is unknown. Petrohyoid muscles
from the anterior margin of the mandible and inserts on are not present in salamanders.
the posterolateral processes of the hyoid. In most anu-
rans, the m. geniohyoideus is composed of medial and Mm. genioglossus and hyoglossus
lateral components, although it is single in Leiopelma and The tongue is composed of two muscles in anurans,
the discoglossids. The muscle protracts the hyoid and is the m. genioglossus and m. hyoglossus (Fig. 13-22). The
associated intimately with the m. sternohyoideus (a de- m. genioglossus basalis is a small muscle that lies in the
rivative of the m. rectus abdominis of the ventral trunk área of the mandibular symphysis above the m. sub-
musculature) which arises from the sternum, inserts along mentalis at the anterior root of the tongue. The m. gen-
the posterolateral edge of the hyoid. and acts to retract ioglossus medialis arises just behind the mandibular sym-
rhe hyoid píate. Movement of the hyoid píate also is physis, dorsal to the m. genioglossus basalis, and is
affected by the m. omohyoideus and the mm. petro- composed of parallel fibers that diverge slightly poste-
hyoidei. The m. omohyoideus is unique to, and present riorly and inserí on hyoglossal fibers. This muscle forms
in most, anurans; it arises from the ventral margin of the the upper surface of the tongue. The m. hyoglossus arises
scapula and inserts on the edge of the hyoid píate. The from the ventral surface of the posteromedial processes
mm. petrohyoidei are derived from the branchial arch of the hyoid, extends along the ventral surface of the
musculature; they arise from the venter of the skull in the hyoid píate, and turns posterodorsally into the floor of
auditory región and attach to the lateral edge and the the mouth at the anterior edge of the hyoglossal sinus.
MORPHOLOGY
324 Fibers of the m. hyoglossus inserí on the fibers of the gorize the observed variation. Thus, Griffiths (1959:
m. genioglossus medialis. The point of its flexión repre- proposed that on the basis of development, anuran ver-
sents the posterior root of the tongue; distal to this root, tebral centra could be classified as ectochordal (spocL-
the m. hyoglossus forms the free ventral surface of the shaped with an open center in which the notochord lies
tongue. holochordal (spool-shaped with solid center), or stegc-
chordal (depressed dorsoventrally and solid). Taking is-
AXIAL SYSTEM sue with Griffiths's scheme, Kluge and Farris (1969) sug-
The axial skeleton provides a rigid, but flexible, longitu- gested that based on developmental evidence providec
dinal brace for the support of the head and viscera and by Mookerjee (1930) and Mookerjee and Das (1939
suspensión of the appendicular skeleton, and serves as anuran centra are either perichordal or epichordal. Per-
a conduit for the spinal cord. If a tail is present, it is ichordal centra are formed from ossification around th¿
supported by the posterior part of the vertebral column. notochord; the resulting centrum thus is cylindrical in cross
The vertebral column is composed of varying numbers section. Epichordal centra are formed from ossificatio'-
of individual vertebrae, each of which consists of a cylin- associated with the dorsal part of the notochord; the re-
drical body of bone known as a centrum which is round sulting centrum tends to be depressed in cross sectior.
or oval in cross section. The neural arch is located on On the basis of rather limited evidence, Kluge and Farrif
the dorsal side of each centrum; the spinal cord passes also noted that there is considerable variation in the de-
dorsal to the centra through the neural arches of the gree of epichordy among anurans; thus some centra are
vertebrae. The neural arch may bear a dorsal projection less depressed than others because ossification extends
known as the neural spine to which muscles and liga- farther down the sides of the notochord. On the basis c:
ments attach. their review of the literature and their own observations
Each vertebra except the first (the atlas, which is lo- Kluge and Farris concluded that anuran vertebrae shouic
cated behind the skull) bears two pairs of processes for be classed as either epichordal or perichordal, and tha:
articulation with adjacent vertebrae; the prezygapophyses Griffiths' term holochordal should be reserved to describí
located at the anterior end of the vertebra articúlate with any centrum that is solid, as opposed to one which is
the postzygapophyses located at the posterior end of the ringlike (i.e., hollow in the center).
next anterior vertebra. In addiüon, amphibian vertebrae Griffiths (1959b) and Kluge and Farris (1969) were
may bear various lateral projections—namely, diapo- concerned with vertebral development and morphology
physes for the attachment of the upper head of two- as it applied to anurans primarily. Other authors, notably
headed ribs, parapophyses for the attachment of the lower E. Williams (1959), D. Wake (1970), and most recently
head of two-headed ribs, and pleurapophyses repre- Gardiner (1983) have taken broader views. Gardiner
senting the rib attachments of the vertebra plus the fused provided a summary of the literature relating to vertebral
rib. The first postcranial vertebra or atlas of all amphibi- development among fishes and tetrapods, and concluded
ans is modified anteriorly to articúlate with the skull. The that in all Recent amphibians the vertebrae are formed
atlas bears two cup-shaped atlantal cotyles that form con- chiefly by membrane bone with only the ends of the
dyloid joints with the occipital condyles of the skull. Ribs centra and the cores of the neural and haemal arches
in amphibians are either present or absent, and if present, being formed of cartilaginous bone. According to Gar-
may bear a double-headed or single-headed articulation diner (1983), initially the vertebra is formed from bone
with the vertebra, or be fused to the vertebra. The ribs produced from the notochordal mesenchyme (perichor-
of amphibians are unique among tetrapods (including dal) that spreads in the perichondrium, the fibrous mem-
labyrinthodont amphibians} because they do not extend brane that covers cartilage. He argued that cartilage be-
beyond the vertebral musculature into the flank muscu- tween adjacent vertebrae forms between the two sheaths
lature (with the exception of some salamanders, e.g., Eu- of the notochord and therefore is chordacentral. Thus, in
proctus and Triturus). As pointed out by Cox (1967), the Gardiner's view, the vertebral centra of amphibians are
presence of short ribs probably is correlated with the perichordal with some chordacentral additions. This con-
mechanism of breathing in amphibians which involves a clusión contrasts with those of Schmalhausen (1958).
buccal pump rather than expansión of the coelom for E. Williams (1959), D. Wake (1970), and D. Wake and
inflation. Lawson (1973), all of whom claimed that in salamanders
In addition to various articulations between adjacent the husklike centrum was the result of perichondral os-
vertebrae described above, successive vertebral centra sification.
articúlate with one another via condyloid joints. Although Amphibian vertebrae also are classified on the basis of
the centra of all Recent amphibians are monospondy- their intervertebral relationship. Thus, the term amphi-
lous, the formation and the appearance of the centra, as coelous is used to describe amphibians having centra that
well as the nature of the articulation between them, are are biconcave terminally and separated by intervertebral
variable. The origin of this variation as well as its func- cartilage which may or may not be independent of the
tional and phylogenetic significance continué to be issues adjacent centra. Opisthocoelous denotes a condition
of debate. Various schemes have been devised to cate- wherein the intervertebral cartilage is confluent with the
 Musculoskeletal System
anterior end of the centrum; thus, a condyloid joint that men magnum of the skull and bears articular facets that 325
alows movement in two planes is formed between the articúlate with the lateral walls of the foramen.
anterior end of one centrum and the posterior end of the The trunk región lies between the atlas and the sacrum,
sr.teriorly adjacent centrum. Procoely ¡s the reverse of and is composed of 10—60 vertebrae depending on the
opcsthocoely; thus, the intervertebral cartilage is associ- species of salamander. Unlike most other vertebrates, the
aoed with the posterior end of each centrum. spinal nerves of salamanders often pass through foramina
The axial musculature is composed of somatíc or par- in the vertebrae, but many salamanders (e.g., hynobiids,
i=t¿ muscles that are derived from the myotomes of the cryptobranchids, and proteiids) also retain intervertebral
epimere (dorsal muscle píate) and innervated by spinal nerves (Edwards, 1976). Trunk vertebrae generally are
nerves. Somatic muscles are constituted by an axial similar to one another (Fig. 13-23), although the centrum
sxcession of muscle segments or myotomes, each of length of midtrunk vertebrae is greater than that of ver-
•hich is separated from the adjacent myotome by a con- tebrae at the anterior end of the column and behind the
nective tissue partition known as a myoseptum. My- sacrum. The functional significance of this and other var-
rxomes are divided in dorsal and ventral halves by a iation in vertebral proportions is discussed by Worthing-
rerizontal skeletogenous septum; the dorsal half com- ton and D. Wake (1972). Zygapophyses are well formed
pnses the epaxial musculature, whereas the ventral half and broad, a neural spine is present, and ribs are present
s tr.e hypaxial musculature. on all but the most posterior trunk vertebrae. Ribs usually
In amphibians, the epaxial musculature consists of a are bicapitate, with the ventral head (capitulum) articu-
srgie. segmented sheet, the m. dorsalis trunci, from which lating with the parapophysis projecting from the dorsal
rnany deeper fiber tracts arise that span two or more part of the centrum, and the dorsal head (tuberculum)
5_ccessive vertebrae. These muscles facilítate angular articulating with the diapophysis which arises near the
T.ovement between vertebrae in the horizontal plañe; midpoint of the neural arch. The diapophyses tend to be
5-;ch movement is associated with lateral undulations of posterolaferally oriented and robust (e.g., Salamandra),
4ie body. and sometimes are termed transverse processes. In some
The hypaxial musculature is composed of three series— salamanders (e.g., some hynobiids, cryptobranchids, and
—e subvertebral, flank (i.e,, lateral), and abdominal mus- plethodontids), the two heads of the rib have fused to
r^es. The subvertebrals are the most dorsomedial and flex produce a unicapitate rib. The ribs of the anterior trunk
r.e spinal column. The flank muscles, or oblique series, vertebrae (second and third) tend to bear cartilaginous
iré composed of three sheets of muscles superimposed expansions at their distal extremities for the attachment
:r. one another. The abdominal muscles extend from the of muscles suspending the pectoral girdle to the vertebral
i-.oulder to the pelvis; the right and left halves of this column.
series are separated by an aponeurosis, the linea alba. The sacrum is an enlarged trunk vertebra with trans-
7ne abdominal and flank muscles provide support for verse processes (diapophyses) and ribs that are elabo-
—e viscera, flex the vertebral column ventrally, and in rated for support of the pelvic girdle (Fig. 13-23). The
se me cases retract the hyoid apparatus. ¡lia of the girdle are bound to the sacrum by fibrous tissue.
The caudal-sacral región consists of two to four ver-
Salatnanders
tebrae posterior to the sacrum (Fig. 13-23). These ver-
Axial Osteology. Most early descriptions of the axial tebrae usually do not bear ribs. The last vertebra of the
skeletons of salamanders as exemplified by Francis (1934) series is distinguished by its possession of a well-devel-
ir.d Hilton (1948, and references cited therein) are ty- oped but nonspinous haemal arch ventrally. This verte-
pological. Interest has been rekindled recently owing to bra supports the posterior part of the cloaca and marks
D. Wake's (1970) and D. Wake and Lawson's (1973) the posterior limit of the trunk of the salamander.
iescriptions of the various kinds of centra and their de- Depending on the species of salamander, the caudal
velopment in salamanders, especially as this relates to or tail región may consist of 20 to more than 100 ver-
relaüonships among Recent amphibia (see also Gardiner, tebrae. These vertebrae exhibit a gradual reduction in
1983, and included references). the sizes of their transverse processes and zygapophyses,
Vertebral regions.—The vertebral column consists of but these structures never are enürely absent. All caudal
rive, poorly differentíated regions—namely, cervical, trunk, vertebrae bear a ventral haemal arch that forms a bony
sacral, caudal-sacral, and caudal regions (Fig. 13-23). The canal for the protection of the caudal artery and vein.
cervical región is represented by a single vertebra, the Tail autotomy is characteristic of most salamanders un-
atlas, that lacks ribs. Unlike other amphibians, in sala- der conditions of stress. The process has been reviewed
manders the atlas bears four points of artículation with and studied by D. Wake and Dresner (1967). Breakage
trie posterior end of the skull (Fig. 13-23). There are two, occurs in an intervertebral plañe and subsequently an-
large, cup-shaped atlantal cotyles that articúlate with the other tail is regenerated. If the salamander has a thick-
occipital condyles. Ventromedially, between the atlantal based tail (e.g., Desmognathus), breakage usually is lim-
cotyles is an anterior process, the odontoid process or ited to the posterior, thinner part of the tail. In species
tuberculum interglenoideum, that projects into the fora- with slender-based tails (e.g., Chioglossa), breakage can
MORPHOLOGY
326

Figure 13-23. Vertebrae of the salamander

Ambystoma opacum, redrawn from Worthington
(1971). A. Atlas in dorsal, B. ventral, and
C. lateral views. D. Seventh trunk vertebra in
dorsal, E. ventral, and F. lateral views.
G. Anterior view of seventh rib drawn to slightly
larger scale than vertebra. H. Sacral vertebra in
dorsal, I. ventral, and J. lateral views.
K. Anterior view of sacral rib drawn to slightly
larger scale than sacral vertebra. L. First caudal
vertebra in dorsal, M. ventral, and N. lateral
views.

occur anywherc throughout the length of the tail, but ¡t appearance of an acellular sheath in the mesenchymc
does so in a specialized manner. The break in the skin around the developing centrum. The sheath rapidly r-
occurs one segment posterior to the break in the muscle; creases in thickness, and becomes cellular as it endoses
thus, the skin covers the wound to facilítate healing. Most connectíve tissue cells. Bone first appears in the ang^s
plethodontid salamanders have constricted-based tails. In between the bases of the neural arch and then spreaás
these species, tail breaks usually occur in the basal, con- over the surface of the notochordal sheath in the cor-
stricted área, at the end of the first caudal segment where nective tissue mesenchyme. In the majority of salamar-
the muscle is thinner and the skin weaker. After auto- ders the bone spreads from the notochordal meser-
tomy, tail regeneration proceeds rapidly with all tissue chyme into the perichondrium of the neural and haemá.
except the notochord being regenerated. arches. Because ossification never separates the cartüa-
Centra.—The centra of salamander vertebrae typically ginous arches from the notochordal sheath, the carti¿-
have been described as either amphicoelous (i.e., bicon- ginous core of the neural arch rests directly in the noto-
cave) or opisthocoelous (bearing a condyle at the anterior chord. In the hynobüd Ranodon, bone penetrales benear
end of the centrum that articúlales with a concavity in the bases of the neural arches, thereby completely re-
the posterior end of the next anterior centrum). Based moving the cartilaginous arch from the notochord bc-
on developmental and histological studies, D. Wake neath (Schmalhausen, 1958).
(1970), Worthington (1971), and D. Wake and Lawson According to Gardiner (1983), while ossification of -.-.•£
(1973) have shown that the structure and relationships centrum and neural arch is progressing, cartilagino'_£
of vertebral centra in salamanders are a great deal more intervertebral rings form and become enclosed within tr.€
complex than has been assumed in the past. The centra ends of two, adjacent centra. However, Schmalhausen
have a dual origin from both cartilaginous and membra- (1958), E. Williams (1959), D. Wake (1970), and
nous components. Gardiner (1983) provided a contro- D. Wake and Lawson (1973) reported that the husklike
versial summary based on the work of other individuáis centrum of salamanders is a perichondral ossification rather
(see Schmalhausen, 1958, and additional references) in than a perichordal ossification as stated by Gardiner. His
which he stated that formation of salamander vertebrae conclusión is based on the fact that the centrum ossifies
begins with the appearance of paired, cartilaginous an- prior to formation of intervertebral chordacentral cartilage
lagen in the position of the myosepta. The dorsal ele- that forms between the two sheaths of the notochord—
ments fuse to form a neural arch dorsally, whereas the a process not observed by D. Wake (1970) or D. Wake
ventral elemente fuse to form a haemal arch in the tail and Lawson (1973).
ventrally. The process of ossification commences with the Once formed, the cartilaginous ring may remain nar-
 Musculoskeletal System
row, or it may widen to fill the intervertebral gap. Ulti- where they arise from, and insert on, bone. In the región 327
mately, two intervertebral configuratíons are possible in of the neck, the m. intertransversarius is differentiated
salamanders. The cartilaginous ring may remain undi- into three muscles that attach to the back of the skull and
vided and the notochord unconstricted, or the ring may that are described above with the neurocranium of sal-
nicken and contrict the notochord intervertebrally. If the amanders. These muscles are the mm. transversarius capitis
ring is segmented transversely, an opisthocoelous joint is superior, posterior, and inferior.
•ormed between adjacent vertebras. Thus the cartilage, Hypaxial musculature.—The hypaxial, or so-called
which may become mineralized or ossified (D. Wake and ventral trunk musculature consists of both dorsal and
Lawson, 1973), adheres to the anterior end of the cen- ventral components that are subdivided into three cate-
rum. The resulting vertebra is composed primarily of gories—subvertebral, flank, and abdominal muscles—all
membrane bone with the cores of the neural and haemal of which are innervated by spinal nerves (Fig. 13-24).
arches, and some parís of the centrum having been formed The subvertebral muscles lie ventral to the vertebral col-
DÍ carülage bone, according to Schmalhausen (1958) and umn, and are composed of at least two sets of muscles.
D. Wake (1970). The most dorsomedial of these is the pars subvertebralis
Primitively, a large notochord persists in salamanders. that is associated with the ventral aspect of successive
Thus the vertebrae of cryptobranchids, for example, are vertebrae. Lateral to these muscles lies the pars trans-
¿escribed as notochordal because the spool-shaped cen- versalis, a band of vertical fibers that are attached to the
oum is hollow, allowing for the passage of the notochord. ventral surfaces of the ribs.
ín more advanced spécies (e.g., ambystomatids) the no- The flank musculature is composed of the oblique
tochord remains continuous throughout life but can be muscles, a series of three muscular sheets that are su-
rather constricted intervertebrally. The cartilage is at- perimposed on one another. The most superficial sheet
tached to the anterior end of each vertebra, and a joint is the m. obliquus externus. The fibers of this muscle slant
is formed by a disk of fibrocartilage with the anteriorly downward posteriorly and arise dorsally from the ribs and
adjacent centrum. Because a kind of condylar joint is the tendinous inscriptions to insert on the next posteriorly
formed, these vertebrae are considered to be functionally adjacent inscription. Beneath this sheet lies the m. obli-
opisthocoelous, but owing to the persistence of the no- quus internus. The fibers of this muscle run in right angles
tochord, they are considered to be notochordal (or am- to those of the m. obliquus externus—that is, they slant
phicoelous) structurally. In more advanced salamanders downward anteriorly. Fibers are attached to adjacent my-
such as salamandrids and plethodonüds, the notochord osepta that are continuous with the ribs. This layer of
may be disrupted almost completely and replaced by flank musculature generally is absent in hynobiid sala-
large amounts of Ínter- and intravertebral cartilage. The manders (e.g., Batrachuperus, Hynabius, and Ranodon)
intervertebral cartilage is highly differenüated and a dis- (Naylor and Nussbaum, 1980). The third and deepest
tínct zone of fibrocartilage marks the articular región be- layer of the flank musculature is the m. transversus, the
tween adjacent centra. The posterior part of the inter- fibers of which run in a dorsoventral directíon and form
vertebral cartilage forms a condyle that is fused to the a band along the flanks. The primary function of the
centrum behind to produce a truly opisthocoelous ver- oblique musculature is to provide support for the vicera,
tebra. and to exert a ventral forcé on the axial column.
The abdominal trunk musculature is represented by
Axial Myology. Among the earliest works dealing with the m. rectus abdominis and its derivatives. This system
the axial musculature of salamanders are those of Maurer of muscles extends between the pectoral and pelvic gir-
{1892, 1911) and Nishi (1916). Francis (1934) included dles and is divided into right and left halves that are
a detailed description of Salamandra salamandra in his separated ventromedially by the linea alba. The most
monograph. More recently, Naylor (1978) dealt with var- superficial layer is the m. rectus abdominis superficialis,
iation in the vertebral column and trunk musculature as an extensive fíat sheet that covers the venter of the ab-
it relates to the systematics of fossil and Recent salaman- domen from the anterior edge of the pubis to the ster-
ders. The description that follows is based primarily on num. The muscle is interrupted by tendinous inscriptions,
Francis's work. each of which is firmly attached to the overlying skin and
Epaxial musculature.—The epaxial, or dorsal trunk, each of which corresponds to a costal groove. The an-
musculature is composed of a superficial, segmented sheet terior fibers of the m. rectus abdominis insert primarily
termed the m. dorsalis trunci (Fig. 13-24). Both this sheet on the posterolateral edge of the sternum and the ante-
and the deeper tracts that are derived from it are inner- rior fibers of the m. rectus abdominis superficialis on the
vated by dorsal rami of the spinal nerves. There are two pericardium; a few fibers extend forward to insert on the
deeper tracts that can be distinguished. The m. interspin- hyoid. Posteriorly, a few fibers insert on the ypsiloid car-
alis lies on the dorsal side of the vertebrae. Fibers arise tilage if it is present. The deeper layer of the m. rectus
from the posterodorsal edge of the postzygapophysis of abdominis (profundus) arises from the anterior edge of
one vertebra and insert along the dorsal surface of the the pubis in Salamandra, but from the ischium in pleth-
neural arch of the posteriorly adjacent vertebra, the mm. odonüds. The muscle also is characterized by the pres-
intertransversarii lie between adjacent transverse processes ence of tendinous inscriptions, the most posterior of which
MORPHOLOGY
328 |—m obliquus externus
-m dorsalis trunci

-m sternohyoideus m rectus abdominis L pelvic girdle

m subvertebralis—i

m obliquus ¡nternus

-m sternohyoideus m transversus abdominis

intervertebral fibers intervertebral fibers

D
myoseptal-
prezygapophysis vertebral
fibers

Figure 13-24. Diagrammatic illustration of

salamander trunk musculature. A. Superficial.
B. Deep to mm. obliquus externus and rectus -m subvertebralis
abdominis. C. Deep to m. obliquus ¡nternus. postzygapophysis—'
D. Dorsal view of epaxial musculature. Adapted
from K. Liem (1977). -intermyoseptal fibers

are attached to the superficial layer of the muscle derivatives of the rectus abdominis muscles, namely the
(m. rectus abdominis superficialis) in most salamanders; mm. ypsiloideus anterior and ypsiloideus posterior. The
anteriorly, the two layers of muscle are not attached. The former muscle is composed of a few fibers that origínate
m. rectus abdominis profundus extends anteriorly to the from the anterior edge of the lateral processes of the
sternum. At this level one portion of the muscle forms a ypsiloid cartilage and inserí on the anteriorly adjacent
neck muscle, the m. rectus cervicus profundus, whereas inscription. Contracüon of this muscle elevates the ypsi-
the remaining fibers (m. hebosteoypsiloideus) pass for- loid cartilage. The m. ypsiloideus posterior is a much
ward to inserí on the urohyal. The primary functions of larger muscle that arises from the anterodorsal edge of
the rectus abdominis muscles are to provide support for the pubis deep to the m. rectus abdominis profundus and
the viscera, retract the hyoid, and flex the vertebral col- spreads anteriorly in a fan shape to insert on the lateral
umn ventrally. edges of the shaft and the posterior edges of the lateral
Salamanders possessing an ypsiloid cartilage (see dis- processes of the ypsiloid cartilage. Contraction of this
cussion under Appendicular System) have two additional muscle depresses the ypsiloid cartilage.
 Musculoskeletal System
••í caudal muscles of salamanders are similar to those A G 329
~r~ body. The anterior part of the caudal musculature
i z¿rnguished as the m. iliocaudalis. The fibers of this
arise from the first two or three caudal vertebrae
insert on the ilium. A tough ligament attaches the V^llini '," i^^/

of the haemal arches of the caudal vertebrae to

Ae sidn below, thereby separating the musculature of
•ch half of the tail. Dorsally, there is a deep longitudinal
in the caudal musculature that accommodates
r,sous skin glands.
Caecilians
Axial Osteology. The only summary of the caecilian
skeleton is that of M. Wake (1980c) in which she
.iewed the pertinent literature, and based on her ex-
tion of Dermophis mexicanas, Ichthyophis gluti-
laosus. and Typh/onectes compressicauda, discussed in-
terspecific variation as well as regional, ontogenetic, and
populational variation in the vertebral column of Der-
mophis. Caecilians have an atlas and 95-285 trunk ver-
tebrae: all caecilians lack a vertebra differentiated as a
, and most lack a tail. All vertebrae except the
and the terminal 3—6 vertebrae bear double-headed
The diapophysis with which the dorsal head (tub-
erculum) of the rib articúlales is borne on the anterior
part of the neural arch, whereas the parapophysis for the Figure 13-25. Vertebrae of the caecilian Dermophis mexicanas.
A. Atlas in dorsal, B. ventral, and C. lateral views. D. Tenth
articulation of the ventral head (capitulum) of the rib usu- vertebra in dorsal, E. ventral, and F. lateral views. G. Near-
afly lies at the extreme anterior end of the centrum. terminal vertebra in dorsal, H. ventral, and I. lateral views.
Redrawn {rom M. Wake (1980c).
Vertebral regions.—There is regional variation in the
features and proportions of the vertebrae (Fig. 13-25).
The atlas bears large atlantal cotyles for articulation with
the occipital condyles of the skull. The centrum and neural medial cartilaginous rod appears beneath the notochord
arch of this vertebra are shorter than those of posterior and becomes divided to form the basiventrals. Accounts
vertebrae, and usually this vertebra lacks a nuchal and of the development of the caecilian vertebral column are
ventral keel, transverse processes and elongate parapo- provided by Marcus and Blume. Mookerjie, and Ramas-
physes. The remaining cervical (i.e., next 19 or 20) ver- wami, as cited by M. Wake (1980c). Presumably the
tebrae have a longitudinal nuchal keel for the attachment process is similar to that described for salamanders. A
of dorsal head musculature. The parapophyses are shorter peripheral cartilaginous ligament joins successive verte-
and more expanded, and the pre- and postzygapophyses bral centra in some taxa. Naylor and Nussbaum (1980)
broader and flatter than those of more posterior verte- suggested that the intercentral ligments, which have no
brae. Midbody vertebrae have well-extended rib-bearers, muscle fibers associated with them, seem to provide au-
narrower zygapophyses, and a greater length than an- tomatic realignment of the vertebrae after flexión and
terior vertebrae. Toward the posterior end of the animal, strengthen the intervertebral joints.
overall vertebral dimensions decrease, and in the cloacal
región transverse processes (and ribs), parapophyses, and Axial Myology. Early contributions to knowledge of
the ventral keel are absent. The most posterior vertebrae caecilian trunk musculature includes Wiedersheim (1879),
consist of rings (composed of the much-reduced centrum Nishi (1916), Marcus (1934), and von Schnurbein (1935).
and neural arch) around the terminal fibers of the spinal There are three basic, recent works that deal with cae-
cord. These vertebrae are shaped irregularly and usually cilian trunk musculature in some detail—Lawson (1965)
fused into sets of two or three vertebrae. on Hypogeophis, and Naylor and Nussbaum (1980) and
Centra.—The centra of caecilian vertebrae are spool- Nussbaum and Naylor (1982) on comparatíve studies of
shaped and amphicoelous. Centrum development is several taxa. The last work is particularly helpful because
initiated by the appearance of a series of paired, cartila- the authors summarize variation among 28 species of
ginous anlagen (i.e., basidorsals) resting above the no- caecilians, summarize early work, provide.a table of syn-
tochord on its outer sheath; the basidorsals may fuse onyms of muscle ñames, and compare the trunk mus-
basally in an anterior-to-posterior sequence to give rise culature of caecilians with that of salamanders and anu-
to two continuous, cartilaginous rods. Subsequently, a rans. The major difference between caecilians and other
MORPHOLOGY
330 amphibians with respect to axial musculature is that all ventrally. Deeper elements of the sheath are the m. ob-
of the hypaxial components except the subvertebral mus- liquus internus laterally and the m. transversus ventro-
culature form an external muscular sheath that is at- laterally. The m. obliquus internus usually is unsegmentec.
tached firmly to the skin by fibrous connective tissues lies between the m. obliquus profundus and m. trans-
and virtually disassociated from vertebral musculature; versus, and has nearly vertical fibers. The m. transversus
thus, the skin and superficial muscles move as a unit. In is a deep, sheetlike, unsegmented muscle with dorso-
caecilians having only primary annuli, or primary and ventral fibers.
secondary annuli (Caeciliidae, Scolecomorphidae, Ty- The most dorsal part of the hypaxial musculature is
phlonectidae, Uraeotyphlidae), the posítions of the pri- the m. subvertebralis which is separable into three parts
mary annuli correspond to the positions of the myosepta The uppermost layer consists of basapophyseal muscles
in this sheath. This congruency is absent in species having that connect successive vertebrae. Each muscle blends
tertiary annuli (Rhinatrematidae, Ichthyophiidae). laterally and ventrally into its associated subvertebr¿
Epaxial musculature.—The epaxial musculature con- myomere, and these myomeres represent a series o:
sists of a thick dorsal mass of V-shaped flexures that ex- overlapping units divided by myosepta deep to the ex-
tend posteriorly, the m. dorsalis trunci (Fig. 13-26). Deep ternal sheath. The most ventral part of the subvertebra!
to this are series of paired hyperapophyseal muscles that musculature, the pars ventralis, is a series of muscles that
origínate over the neural arch of one vertebra and insert attach midventrally to the vertebral centra and subcentral
by a broad aponeurosis to the hyperapophysis of the keels, and extend anterolaterally to insert on the externa!
anteriorly adjacent vertebra ¡n a manner characteristic of muscular sheath. This layer of subvertebral muscles is
salamanders. unknown in salamanders and anurans.
Hypaxial musculature.—The hypaxial components Although the trunk musculature ¡s basically similar to
of the muscular body wall sheath are the mm. obliquus that of salamanders, it is much better developed in cae-
externus superficialis, rectus lateralis, obliquus externus cilians. Moreover, caecilians possess a derivative of the
profundus, rectus abdominis, obliquus internus, and m. subvertebralis unknown in salamanders, and the ver-
transversus (Fig. 13-26). The m. obliquus externus su- tebral musculature is largely independent of the body
perficialis forms a narrow, longitudinal band of muscles wall muscles in contrast to all salamanders except Am-
on the dorsolateral edge of the body; the fibers are ar- phiuma means. Nussbaum and Naylor (1982) correlatec
ranged in an oblique plañe, and may or may not be these differences with the locomotory habits of caecilians
segmented. This band covers the junction of the two that involve serpentine and vermiform actíon, both of
deeper components of the sheath—the m. rectus lateralis which are possible only if the vertebral column is supple
dorsally, and the m. obliquus externus profundus ven- and the trunk muscles well developed.
trally. The former ¡s a longitudinal, segmented band of
muscles, whereas the latter is a sheetlike muscle having Anurans
fibers that extend longitudinally between the myosepta. Axial Osteology. The axial skeleton of anurans is highly
Ventromedially, the sheath is composed of the seg- modified in comparison to those of salamanders and cae-
mented m. rectus abdominis. This muscle is continuous cilians; moreover, there is a great deal of variation in
with the m. obliquus externus profundus dorsally, and centrum structure. Doubtless, it was this variation that
separated into right and left halves by the linea alba mid- attracted the attentíon of many earlier workers. Thus.

m dor trunci—i
m subvert—¡
i—m rect lat basapophyseal muse

rect lat

m obl ext
super
Figure 13-26. Schematic illustration of m obl ext
caecilian trunk muscles redrawn from Nussbaum prof
and Naylor (1982). Abbreviations: m dor m obl int
trunci = m. dorsalis trunci; m obl ext prof = m transv
m. obliquus externus profundus; m obl ext
super = m. obliquus externus superficialis; m
obl int = m. obliquus internus; m rect abdom = rect abdom
m. rectus abdominis; m rect lat = m. rectus
lateralis; m subvert = m. subertebralis; m
transv = m. transversus; m vert pars vent =
m. subvertebralis pars ventralis; muse = L-m obl ext prof m vert pars vent—'
muscle. -m obl ext super
 Musculoskeletal System
Cope (1865) and Noble (1922) used vertebral characters rans the arch is complete and bears a neural spine. Gen- 331
E their major classifications of anurans. Nicholls (1916), erally, neural spines are best developed on anterior pre-
Hookerjee (1931), and Griffiths (1963) investigated the sacrals and gradually diminish in size posteriorly.
«xphology and development of anuran centra, and de- Depending on the posterior elaboraüon of the neural arch,
sesoped a scheme of classificatíon of vertebral types that the presacral vertebrae may be nonimbricate (i.e., non-
subsequently was amended by Kluge and Faros (1969). overlapping as in Ascaphus) or imbrícate (i.e., overlap-
Most recentíy, Gardiner (1983) has reviewed vertebral ping as in pipids).
oeveiopment in anurans as part of his review of gnath- In many anurans, there is a tendency to reduce the
oaome vertebrae and the classification of the Amphibia. number of presacral vertebrae through fusión. The centra
ite these efforts, there is still a great deal to be learned of Presacrals I and II fuse (e.g., Pipa, Fig. 13-27B), and
at the ontogenetic and adult variation in anuran ver- the atlas comes to bear a pair of transverse processes.
: ;-: and its functional and phylogenetic significance. Fusions can involve as many as the first four presacrals
Vertebral regions.—The anuran vertebral column (e.g., some dendrobatids). The number of presacral ver-
r^stomarily is divided into three regions—presacral, sac- tebrae also is reduced by incorporation of posterior ver-
. and postsacral (Fig. 13-27). The presacral región con- tebrae into the sacrum. When this occurs (e.g., the pipids
• of five to eight vertebrae, the most anterior of which Hymenochirus and Pseudhymenochirus), it is evidenced
; —.e atlas or cervical vertebra (also designated as Pre- by the presence of additional spinal nerve foramina in
sacral I). The atlas lacks transverse processes in most the sacrum.
arurans, and bears a pair of atlantal cotyles that articúlate Ribs occur in only three Recent anuran families—leio-
«t±i the occipital condyles of the skull. The odontoid pelmatids, discoglossids, and pipids—and usually are lim-
process of salamanders is lacking in anurans. ited to three pairs that are associated with the transverse
Each presacral vertebrae posterior to the atlas bears a process of Presacrals II, III, and IV (Fig. 13-27). Occa-
pair of pre- and postzygapophyses on the neural arch, sionally, the leiopelmatids have a fourth pair of ribs as-
2¡-.d a pair of transverse processes (parapophyses) that sociated with Presacral V. The ribs are free in the leio-
scend laterally from the pedicel. The transverse processes pelmatids and discoglossids, but ankylosed to the
:•: Presacrals II-IV or V are expanded and more robust transverse processes in adult pipids.
r-an those of the posterior presacrals, and bear muscular The sacrum usually is a single, specialized vertebra (but
irachments for the suspensión of the pectoral girdle. see discussions of vertebral fusions above) from which
There is considerable variation in the development of the pelvic girdle is suspended. It is located between the
—2 neural arches of presacral vertebrae. In poorly ossi- presacrals anteriorly and the rodlike coccyx ( = urostyle)
ied species (e.g., Notaden) the halves of the neural arch posteriorly. The sacrum bears a pair of prezygapophyses
•r.ay fail to unite on anterior vertebrae, but in most anu- which articúlate with the postzygapophyses of the last

Figure 13-27. Anuran vertebral

columns in dorsal view. A.
truel illustrating a frog with
nonimbricate vertebrae, free ribs, a
sacrum with moderately expanded
diapophyses, and vestigial processes
on the coccyx. B. Pipa myersi, an
example of a species having only six
imbrícate presacral vertebrae with
the first two presacrals fused, ribs
that are ankylosed to the transverse
processes, a sacrum with widely
expanded diapophyses, and the
sacrum fused to the coccyx.
C. Leptodactylus pentadactylus, a
species with eight presacral
vertebrae, most of which are
nonimbricate, a sacrum bearing
diapophyses that are scarcely
expanded, and moderately broad
transverse processes. D. Rana
escalenta, an anuran with nearly
round, posterolaterally oriented
sacral diapophyses.
MORPHOLOGY
332 presacral vertebra, but postzygapophyses are absent on centrum. The term diplasiocoelous has been used to c£-
the sacra of almost all anurans (Fig. 13-27). The trans- scribe the condition typical of most microhylids, ranids.
verse processes of the sacrum are expanded to form sac- hyperoliids, and rhacophorids in which all but the lar
ral diapophyses that articúlate with the ilia of the pectoral presacral vertebra are procoelous. The last presacral ^
girdle. The sacral diapophyses are broadly expanded in biconcave; thus, it bears a normal procoelous relationshir
some anurans (e.g., pipids and some pelobatíds), mod- with the anteriorly adjacent vertebra, but articúlales wi™.
erately dilated (e.g., bufonids, hylids) in many, and round a condyle produced at the anterior end of the sacrurr.
or cylindrical in some (e.g., ranids, pseudids). posteriorly.
The terminal element in the anuran axial column is the Based on developmental evidence, Griffiths (1959a.
coccyx (Fig. 13-27), a rodlike element that represents the 1963) proposed another classification of anuran vertebra!
fusión of postsacral vertebral elements. The coccyx lies centra. In the embryo, sclerotomic cells aggregate aroun;
between the shafts of the ilia of the pelvic girdle and bears the notochord to produce a perichordal tube. The centra
muscular attachments to these elements. In most anurans and intervertebral bodies develop as thin (centra) and
the coccyx bears a bicondylar articulation with the sa- thick (intervertebral bodies), alternating, cylindrical seg-
crum, although in some (e.g., pipids) it is fused or bears ments along the length of the continuous perichordal tube
a monocondylar articulation (e.g., Rhamphophryne). In surrounding the notochord in all anurans. Subsequer.:
leiopelmatids, the coccyx lacks a distinct articulation with development occurs in one of four ways to produce three
the sacrum, and instead, the two components are con- different types of centra. If the entire perichordal sheatr.
nected by fibrocartilage. A dorsal crest and lateral ex- is converted to cartilage and then bone, the resulting
pansions are variably developed on the urostyle, and in centrum is an ossified cylinder that endoses a persisten:
some anurans (e.g., pelobatids, and some leptodactylids notochord. This condition ís termed ectochordal anc
and bufonids) the anterior end may bear a pair of ves- characterizes leiopelmatids and Rhinophrynus. In some
tigial transverse processes. pelobatids and some advanced frogs, the notochord :;
Centra.—The structure of the vertebral centra in anu- replaced completely by bone so that the centrum is cyl-
rans is highly variable, and although several schemes have indrical and solid; such vertebrae are described as hol-
been devised to categorize this variation, none is partic- ochordal. Stegochordal vertebrae, in which the centra are
ularly amenable to phylogenetic, functional, or ontoge- transversely flattened rather than cylindrical, arise in one
netic interpretation. The terms most frequently encoun- of two ways according to Griffiths. In pipids and some
tered in the literature describing anuran centra are pelobatids, a cartilaginous perichordal sheath is formed
amphicoelous, anomocoelous, opisthocoelous, procoe- in the same manner as for ectochordal and holochord¿
lous, and diplasiocoelous, especially as these were pro- vertebrae, but ossification is limited to the dorsal part of
mulgated by Noble (1922, based on the work of Nicholls, the cylinder. The lateral and ventral parís of the cartila-
1916) in his classificatíon of frogs. Amphicoelous has been ginous perichordal tube degenerate. In discoglossids, both
applied to primitive anurans (e.g., leiopelmatids) in which chondrification and ossification are limited to the dorsal
the bony centrum is terminally fíat or biconcave, rem- part of the perichordal tube; the rest of the tube remains
nants of the notochord persist, and the intervertebral joint fibrous and finally degenerates at metamorphosis.
(including that between the sacrum and urostyle) is formed Griffiths's work was based in part on that of Mookerjee
by a combination of hyaline and fibrocartilage. The term (1931) and Mookerjee and Das (1939), who defined two
anomocoelous has been used to describe the pelobatids, primary modes of centrum development—perichordal and
in reference to the relationship of the coccyx and sacrum epichordal. Perichordal formation includes (1) conden-
which either are fused or have a monocondylar articu- sation of sclerotomic cells around the notochord to form
lation in this family. The presacral centra have a variety a notochordal sheath that subsequently chondrifies, and
of configurations in pelobatids. They may be biconcave (2) partial or entire replacement of the notochordal car-
with a free intervertebral disc that remains cartilaginous tilage by bone. This mode of development thus would
or is mineralized. The disc may tend to adhere to the include Griffiths's ectochordal and holochordal vertebral
posterior end of the centrum without actually being fused types. Mookerjee's epichordal vertebral development is
to it, or it may be united synostotically with the centrum equivalent to Griffiths's stegochordy in the discoglossids
to form a procoelous vertebra (see definition below). Op- because chondrification and ossification occur only in the
isthocoely refers to a condition in which the presacral dorsal and dorsolateral áreas of the perichordal tube of
centra are concave posteriorly and bear a condyle formed sclerotomic cells. The relative merits of these two systems
from intervertebral cartilage on their anterior ends for of anuran vertebral classification were discussed at length
articulation with the anteriorly adjacent centrum. This by Kluge and Farris (1969) who preferred to desígnate
pattern is typical of discoglossids and pipids. In procoe- centra as either epichordal or perichordal (sensu Mook-
lous anurans (the fossil palaeobatrachids, some peloba- erjee, 1931), and retain Griffiths's term holochordal in
tids, and all other more advanced frogs), the presacral reference to vertebrae in which the notochord is replaced
centra are concave anteriorly and bear a condyle on their entirely by bone. Logic suggests that the term notochor-
posterior end for articulation with the posteriorly adjacent dal (as used by D. Wake, 1970) could be used to describe
 Musculoskeletal System
.crtebrae in which remnants of the notochord persist. umns and greatly reduced vertebral and body wall mus- 333
The most recent contriburion to this controversy was culature as compared with caecilians and salamanders.
made by Gardiner (1983). He pointed out that, as in These differences in the axial musculoskeletal system seem
salamanders, centrum formatíon in anurans begins with to be correlated with the development of saltatorial lo-
—e appearance of paired basidorsal cartilages in the po- comoüon in anurans whereby the organisms rely on
srron of the myosepta. From this point there are two powerfully developed hindlimbs for progression in both
possible courses for further development that result in terrestrial and aquatic environments. Obviously, undu-
perichordal or epichordal vertebrae, respectively. In the latory movements are not involved in saltatorial loco-
case of perichordal vertebrae, the basidorsal cartilages motion; therefore, spinal flexión is of minimal importance
T_s€ basally to form two continuous longitudinal rods, to the animal. Moreover, too much axial flexibility would
-.hereas the basiventrals take the form of a median rod be detrimental to an organism that relies on trajecting its
:: cartílage or a hypochord. The rod may subdivide (as rigid, fusiform body forward by means of the hindlimbs.
't does in caecilians), but often it persists in the coccygeal Epaxial musculature.—The epaxial, or dorsal trunk,
región. Rings of bone develop in the membrane investing musculature is represented by a series of long muscles in
r.e notochord. Ossification of the centra and neural arches contrast to the relatively homogeneous m. dorsalis trunci
rroceeds separately. Large transverse processes grow out of caecilians and salamanders. The m. longissiumus dorsi
rom the side of the neural arch and extend into the septa is a segmented muscle that originales along the anterior
Detween myomeres. According to Gardiner, in epichor- part of the coccyx and extends forward along the neural
dal development the basidorsals are the only cartilagi- spines of the presacral vertebrae to insert on the neural
-.ous elements that are formed; he noted, however, that spines and transverse processes of the anterior presacrals
E Williams (1959) and D. Wake (1970) claimed that (Fig. 13-28). Posteriorly, the m. coccygeosacralis origi-
both lateral and ventral cartilages are present, but that
:r.ey degenerate to varying degrees and in some cases
ne basiventrals disappear altogether. Ossification en-
doses the notochord in a membrane bone cylinder which
subsequently grows up over the neural arches and trans-
verse processes. As in salamanders and caecilians, Gar-
riner claimed that intervertebral cartilage forms in the
-otochordal sheath and grows inward to constrict and m itr m lev mand post long
eventually oblitérate the notochord. Subsequently, the cap ¡nf
m itr cap sup
cartilage is divided in a transverse, arc-like plañe at its
anterior or posterior end. The cartilage then ossifies to m icrur
form an articular end that fuses with either the anterior
end of the centrum (opisthocoelous) or the posterior end m itr
procoelous).
By referring to Kluge and Farris's (1969) summary of -m iliolum
anuran vertebral characteristics as well as the summary
presented in Table 17-3, it is obvious that there is a dis-
m long dor
tressing lack of concordance among the various schemes
m coccsac
rhat have been proposed to classify frog vertebrae. More-
over, one must take care to understand precisely the m cocciliac
sense in which various authors are applying descriptive
coccyx
terms. Until much more descriptive morphology based
on histological examination of adult and developing anu- ilium m iliac ext
ran vertebrae has been completed, it will not be possible m tens fas lat
to speculate on the evolutíonary significance of the var- m glut mag
iation that has been observed. -m pyr

Axial Myology. With the exception of Ritland's (1955)

\e 13-28. Dorsal view of the b
account of the postcranial myology of Ascaphus, and the
recent work of T. C. Burton (1983a, 1983b) on micro- redrawn from Gaupp (1896). Superficial muscles removed on left
hylids and M. Davies and T. C. Burton (1982) on Rheo- side. Abbreviations: m cocciliac = m. coccygeoiliacus; m
batrachus silus, the axial musculature of anurans largely coccsac = m. coccygeosacralis; m glut mag = m. glutaeus
magnus; m icrur = m. intercrurales; m ileolum = m. ileolumbaris;
has been overlooked since Gaupp's (1896) and Grob- m iliac ext = m. iliacus externus; m itr = m. intertransversarius; m
belaar's (1924) monographs on Rana and Xenopus, re- itr cap inf = m. intertransversarius capitis inferior; m itr cap sup =
m. intertransversarius capitis superior; m lev mand post long =
spectively. As pointed out by Nussbaum and Naylor m. levator mandibulae posterior longus; m tens fas lat = m. tensor
(1982), anurans have relatively inflexible vertebral col- fasciae latae.
MORPHOLOGY

334 nates from the lateral surfaces of the anterior half of the Deeper epaxial muscles include the mm. intertrans-
coccyx and passes forward to insert on the neural arch versarii dorsi that extend between adjacent transversa
of the sacrum and the sacral diapophyses. The m. coc- processes of the vertebrae and anteriorly form the twc
cygeoiliacus also originales from the lateral surfaces of cervical muscles, the mm. intertransversarii capitis supe-
the coccyx, but its fibers insert along the medial margins rior and inferior. The mm. interspinales ( = mm. intercru-
of the ilia. The final long muscle of the back is the rales of Gaupp, 1896) pass between the neural archs o:
m. iliolumbaris which originales from the anterior extrem- adjacent vertebrae.
ity of the ilium and extends forward to insert on the trans- Hypaxial musculature.—The hypaxial musculature is
verse processes of Presacrals IV—VII. limited to flank and abdominal muscles (Fig. 13-29). Ir.

dep mand
-m dor scap -m transv
-m lat dor m iliac ext- m glut rra;
A -fascia dor
ilium tens
fas la:

hyoid

obl ext
m pect (p abdom)
-m cbl ext (p scap) m sternhyd
-m corbrach brev sternum
-m anc
-m delt -mandible
C m mtermand
clavicle m delt (p epistern)
coracoid m coracorad
m interhyd— H-p episternj
m omohyd m delt (p Scap)
m sternohyd (p epicor p scap > m de:
m m pect clavj
coracorad (p abdom)
m transv
m obl (p scap)
m fl carp rad m corbrach
brev
m pect (p stern) m corbrach
m obl ext long
m pect
(p abdom)

m rect abdom

Figure 13-29. Body wall and pectoral girdle musculature of Rana escalenta, redrawn from Gaupp (1896).
A. Lateral view, superficial. B. Lateral view with shoulder muscles and superficial lateral and ventral
muscles removed. C. Ventral view with pectoral muscles removed on frog's leu side. D. Ventral view
showing deep pectoral musculature on frog's left side and deeper body wall musculature. Abbreviations:
fascia dor = fascia dorsalis; m anc — m. anconeus; m corbrach brev = m. coracobrachialis brevis;
m corbrach long = m. coracobrachialis longus; m coracorad = m. coracoradialis; m crural = m. cruralis;
m delt = m. deltoideus; m dep mand = m. depressor mandibulae; m dor scap = m. dorsalis scapulae;
m fl carp rad = m. flexor carpí radialis; m iliac ext = m. iliacus externus; m interhyd = m. interhyoideus;
m intermand = m. intermandibularis; m lat dor = m. latissimus dorsi; m obl ext = m. obliquus externus;
m omohyd = m. omohyoideus; m pect = m pectoralis; m rect abdom = m. rectus abdominis; m
sternhyd = m. sternohyoideus; m tens fas lat = m. tensor fasciae latae; m transv = m. transversus; p clav
= pars clavicularis of m. deltoideus; p epistern = pars episternalis of m. deltoideus; p scap = pars
scapularis of m. deltoideus; p abdom = portio abdominalis of m. pectoralis; p epicor = portio epicoracoidea
of m. pectoralis; p stern = portio sternalis of m. pectoralis; vag rect = vagina recti.
 Musculoskeletal System
asi to salamanders and caecilians, anurans lack any erally, dorsal to the m. rectus abdominis. At the lateral 335
tebral musculature. There are two layers of flank edge of the m. rectus abdominis the muscle folds around
the m. obliquus externus and m. transversas; the abdominal muscle or folds on its own ventral surface
middle layer of other amphibians, the m. obliquus so that the fibers pass anteriorly over the ventral surface
ñus, is absent. The m. obliquus externus originales of the abdominal muscle, or along the lateral edge of the
the posterior margin of the suprascapula, and the m. rectus abdominis. In the latter case the muscle inserts
ensheathing the epaxial musculature. The broad on the lateral body wall, and in the former the muscle
: of muscle extends posteroventrally to insert along inserts on the skin medially about half way between the
lateral margin of the fascical sheath that invests the pectoral and pelvic girdles. Dorsally, the m. coccygeo-
rolateral surface of the rectus muscle and the ilium. cutaneus originales from the posterior extremity of the
deeper m. transversus arises from the transverse coccyx; apparently this muscle is connected with the rec-
:ess of Presacral IV and the fascia covering the mm. tal musculature from which it passes outward to insert on
rBErtranversarii. This muscle inserts ventrally on the sheath the skin. This muscle is known to occur in Rana; its dis-
ac the m. rectus abdominis anterior to the level of the tribution among other anurans is unknown. A second
aemum and then by a fascical sheet that lies along the muscle, the m. cutaneus dorsalis, arises from the fasciae
nemal surface of the coracoid and scapula. attached to the pubic symphysis, passes dorsally through
The longitudinal fibers of the m. rectus abdominis are the gap between the belly and thigh muscles, and then
ieparated midventrally by the linea alba. Each half of the radiales anteriorly to insert on the skin. This muscle is
—úsele arises by a strong tendón from the ventral border known in microhylids, ranids, hyperoliids, rhacophorids,
rf ríe pubis and passes forward. Anteriorly, the m. rectus and some leptodactylids (T. C. Burlón, 1980).
2¿xiominis widens to cover the abdominal región, and in
r.€ pectoral región the muscle splits into medial and lat-
srai portions. The medial part inserts on the dorsal sur- APPENDICULAR SYSTEM
ace of the sternum and a tendinous inscription lateral to The pectoral and pelvic girdles together wilh Iheir asso-
—e sternum and gives rise to the m. sternohyoideus. The ciated limbs constitute the appendicular skeleton. The
— sternohyoideus arises from the deep surface of the girdles are suspended from the axial skeleton, and Ihe
scemum and attaches to the hyoid anteriorly. In a few limbs, in lurn, articúlate with the girdles. The girdles of
ir.urans (e.g., discoglossids) there is a second derivative modern amphibians are much reduced from those of
rom the medial portion of the m. rectus abdominis, the primiüve terrapods, and in some cases (caecilians) lacking
—. sternoepicoracoideus, which arises from the style of completely.
—e sternum and passes medial to the epicoracoid píate The pectoral girdle lies just behind the head and is
::' the pectoral girdle. The lateral part of the m. rectus divisible into Ihree general áreas. The bladelike supra-
abdominis forms the lateral portion of the m. pectoralis scapular portion lies dorsolateral in Ihe shoulder región
abdominalis, a muscle of the shoulder girdle. In Asca- above the glenoid cavity and bears muscle artachments
phus, which possesses an epipubis, the m. rectus abdom- to the first three or four vertebrae. Lalerally, Ihe glenoid
;nis is differentiated into a prepubic segment that has a cavity for the articulation of the forelimb is formed by Ihe
broad, fleshy origin from the cartílaginous ledge of the scapula and coracoid (and Ihe clavicle in anurans). The
pubis just dorsal to the epipubic píate. This muscle inserts venlral (i.e., abdominal) portions of Ihe pectoral girdle
on the surface of the prepubis and supports the epipubis. can be defined as zonal elements thal support Ihe viscera
Cutaneous musculature.—As T. C. Burton (1980) in part and serve as an attachment site for muscles of the
pointed out in his review of cutaneous muscles in micro- head and trunk regions.
hylid frogs, anurans are unique among tetrapods in hav- The pelvic girdle lies at the end of Ihe Irunk and artic-
ing loóse skin that is attached to the body wall only at úlales wilh Ihe sacral vertebra of the axial column. It is
intervals. One of the forms of attachment is by thin, composed of three pairs of elemente—Ihe ilia, ischia, and
sheetlike cutaneous muscles that insert on the skin. These pubes. The ilium articúlales with the sacrum proximally.
muscles are associated with both dorsal and ventral trunk lis dislal portion forms one facel of the acetabulum for
musculature. In many species of anurans, the lateral por- Ihe articulalion of the próxima! hindlimb bone laterally.
tion of the m. rectus abdominis adheres directly to the The ventral portion of Ihe girdle in salamanders and Ihe
skin. However, in some microhylids the lateral portion of posterior part in anurans is composed of Ihe ischia and
the m. pectoralis abdominalis is a fíat, rectangular slip of pubes.
muscle that originales from the skin; in others this slip of Five basic segmente compose Ihe lelrapod limb; in a
muscle is absent, but the entire m. pectoralis abdominis proximal lo dislal sequence Ihese are Ihe propodium,
is bound to the skin by connective tíssue. Two additional epipodium, mesopodium, melapodium, and phalanges.
cutaneous muscles are associated with the ventral mus- In amphibians, Ihe propodium is represenled by Ihe hu-
culature in some microhylids and ranids. The m. rectus merus (forelimb) and fémur (hindlimb). These are asso-
abdominis pars anteroflecta arises from the pubis anterior ciated, in lurn, wilh Ihe radius and ulna, and Ihe libia
to the origin of the m. rectus abdominis and passes lat- and fíbula—Ihe epipodial elemente of Ihe fore- and hind-
MORPHOLOGY
336 limb, respecüvely. The radius and tibia are located on functional distinction chiefly affects the proximal elemerts
the inner or preaxial (i.e., primitively anterior) sides of (i.e., upper and forearm, and thigh and shank) of the
the limbs. Mesopodial components form the wrist (i.e., limbs; distal muscles are affected little and, in fact, are
carpus) and ankle (i.e., tarsus), and are composed of similar in the fore- and hindlimbs. The musculatures c:
several series of small bones. Proximally, these include the fore- and hindlimbs are generally similar to one an-
the ulnare, intermedium, and radíale of the hand and the other in being composed of short, deep muscles tha:
fibulare, intermedium, and tibíale of the foot. There is a extend over one limb joint, and of longer, more super-
central row of bones, the centralia, and a distal row of ficial muscles that extend over two or more limb seg-
carpalia (hand) or tarsalia (foot). The palm of the hand ments.
and the solé of the foot are composed of metapodial
elements—four metacarpals ¡n the hand and either four Salamanders
or five metacarpals in the foot. The terminal elements are The most complete description of the appendicular
the phalanges, longitudinal series of small bones that form musculoskeletal system of a salmander probably is the:
the digits of the hand and foot. Digits are designated by of Francis (1934) on Salamandra salamandra; earlier lit-
Román numeráis with the first being the preaxial or inner erature is cited in this work. The descriptions of muscles
digit, and the last the postaxial or outer digit. Reduction and their patterns of innervation that follow are based or.
in the number of digits occurs postaxially; thus, when Salamandra. More recent contributions include those of
fewer than five digits are present (hands of all amphibians Hilton (1945, 1946a, 1946b) on ambystomatids, di-
and the feet of some salamanders), one can assume that camptodontids, and plethodontids, and D. Wake (19661.
reduction has occurred through loss of the fifth, or outer, Hanken (1982, 1983), Alberch (1983), and Alberch and
digit. Gale (1985) on plethodontids. Hilton's and Wake's works
As Radinsky (1979) pointed out, the occurrence of are largely descriptive, whereas that of the other authors
girdles and paired appendages interrupts the series of deals with variation in mesopodial and phalangeal ele-
axial myotomes, and the musculature that is associated ments. Aspects of limb development and a review of the
with these skeletal elements is derived from muscle buds literature on this subject was provided by de Saint-
sent out by adjacent myotomes. This musculature tends Aubain (1981). The limbs and girdles are complete in all
to spread over the segmented, axial musculature. This is salamanders except the sirenids and amphiumids. In the
especially true of muscles associated with the pectoral latter, girdles are retained, but the limbs are vestigial.
girdle. Because the girdle lacks a solid attachment to the Sirenids have a pectoral girdle and small forelimbs, but
vertebral column, robust hypaxial muscles extend from the pelvic girdle and hindlimbs are absent.
the ribs and/or transverse processes and the skull to sus-
pend the pectoral girdle from the axial column. The pel- Pectoral Girdle Structure. The pectoral girdle of sal-
vic girdle, in contrast, bears strong fibrous attachments amanders is largely unossified and lacks dermal com-
to the axial column, and although hypaxial muscles ex- ponents (i.e., clavicle of anurans). Each half of the girdle
tend between the pelvis and the fémur, their function is forms a single skeletal element that consists of three áreas—
to move the fémur in the hip joint rather than support the scapular, procoracoid, and coracoid regions—and the
the girdle. halves of the girdle overlap and move freely over one
The primary function of the forelimbs in amphibians is another midventrally (Fig. 13-30). The scapular región
to raise and stabilize the body, although they also help lies dorsolateral to the glenoid fossa (for articulation of
to control movement and velocity, and supplement the the forelimb), and consists a proximal, bony scapula and
power of forward movement supplied by the hindlimbs. a distal cartilaginous píate, the suprascapula. The su-
The primary function of the hindlimbs is to provide forcé prascapula is fan-shaped and attached to the axial skel-
for forward progression. Owing to these functional dif- eton by muscles and connective tissue. The scapula forms
ferences, the basic arrangements of the limbs are differ- the lateral facets of the glenoid cavity, and is united syn-
ent. Thus, the elbow joint of the forelimb is directed back- ostotically with the coracoid that forms the anterior and
ward, whereas the knee joint of the hindlimb is directed medial margins of the glenoid cavity in adult salaman-
forward in order to provide better purchase for the hind- ders.
limb on the substrate. In the case of both the fore- and The ventral portion of the girdle can be divided into
hindlimb, the musculature is composed of basically two the procoracoid and coracoid regions. The procoracoid
groups—dorsal and ventral. In the forelimb, with the el- is a spatulate element extending anteriorly from the gle-
bow joint directed posteriorly, the dorsal or preaxial mus- noid fossa. If it is ossified, it is fused to the scapula in the
cles are the extensors, whereas the ventral or postaxial región of the fossa, but cartilaginous anteriorly. The an-
muscles are the flexors. The situation is reversed in the teromedial margin of the girdle bears a deep notch, the
hindlimb in which the knee joint is directed anteriorly. incisura coracoidea, that separates the cartilaginous re-
The dorsal, preaxial muscles form the flexors, whereas gions of the procoracoid and coracoid. The coracoid re-
the ventral postaxial muscles constitute the extensors. This gión lies posterior to this notch. The coracoid is ossified
 Musculoskeletal System
337

glenoid cav- scapula

'-suprascapula
*— supracoracoid f

3o r
jmen

Figure 13-30. Anterior

appendicular skeleton of Salamandra
salamandra, redrawn from Francis
(1934). A. Right half of pectoral
prepollex girdle in ventrolateral view and
radíale rradlus B. dorsomedial view. C. Ventral
aspect of sternum. D. Right humerus
humerus in dorsal aspect and E. ventral
aspect. F. Right ulna illustrated from
dorsal, G. postaxial, and H. ventral
surfaces. I. Left forearm and hand in
dorsal view. Cartilage is stippled.
Abbreviations: cav = cavity; con =
IV condyle; cpl(s) = carpal(s); cr =
crista; dor = dorsalis; f = foramen;
cpl 4-J L ulnare + intermedium p = process; vent = ventralis.

around the glenoid fossa, but its largest, medial portion of the coracoid plates; these plates are bound to the ster-
is a cartilaginous píate that overlaps its complement on num by connective tissue. The sternum provides some
the opposite half of the girdle. The ossifications of the support for the overlying viscera and serves for the at-
scapular, procoracoid, and coracoid regions are fused tachment of muscles.
completely in adults; thus, many authors refer to the sin-
gle bone as the scapulocoracoid. The bone bears a single Forelimb Structure. The forelimb of salamanders
foramen (supracoracoideum) through which the supra- consists of a humerus proximally, and radius and ulna
coracoideus nerve and its corresponding artery and vein distally (Fig. 13-30); usually the epiphyses of these long
pass. The glenoid fossa is bony except for its ventral, bones fail to ossify. The number of mesopodial elements
posteromedial edge that is formed by the coracoid car- tends to be reduced through loss and fusión, and many
tílage.
of those that remain are cartilaginous. Four metapodial
The sternum is a small, ventral, cartilaginous píate that elements (metacarpals) are present in associatíon with the
lies posterior to the pectoral girdle (Fig. 13-30). The ster- four digits. The most common phalangeal formulae of
num is diamond-shaped. The anterior edges of the ster- the digits is 1-2-3-2 or 2-2-3-3 for Digits I-IV, respec-
num are grooved to receive the posteromesial margins tively, but in some salamanders (notably the plethodon-
MORPHOLOGY
338 tids) reduction occurs. Reduction involves the length of M. cucullaris
the digit, not the number of digits, and is the result of The major muscle attaching the pectoral girdle to the
shortening of the phalangeal elements and occasionally skull is the m. cucullaris which is innervated by C.N. XI
the loss of an element. (accessory) and divided into two heads (Fig. 13-31). The
posterior head (m. cucullaris minor) arises from the dors¿
Musculatura of Pectoral Girdle and Forelimb. The fascia of the head and inserts on the lateral border of the
muscles of the shoulder and forelimb can be separated procoracoid and scapula. The anterior head (m. cucul-
into three groups for discussion—those which attach the laris major) arises in part from the dorsal fascia and in
pectoral girdle to the skull and axial column, and the part from the posterodorsal surface of the skull; it inserts
extensors and flexors of the forelimb. on the lateral face of the procoracoid, near the shoulder
Suspensory muscles of the pectoral girdle.—Among joint, and along the ventral edge of the scapula. Con-
the muscles that attach the pectoral girdle to the skull and traction of this muscle turns and depresses the head un-
vertebral column are the m. levator scapulae (see dis- less the head is immobilized by contraction of trunk mus-
cussion under Neurocranium in Skull and Hyobran- culature that attaches to the posterior end of the skull. In
chium), the m. cucullaris, and the m. thoraciscapularis the latter case, contraction of the m. cucullaris pulís the
(Fig. 13-31). Although the m. levator scapulae arises from pectoral girdle toward the skull.
the otic región and inserts on the suprascapula, it seems
to be involved in the auditory apparatus. Thus, its struc- M. thoraciscapularis
ture is discussed in association with the neurocranial ele- The m. thoraciscapularis arises by a series of bundles
ments of the skull. from the first five ribs and inserts on the medial face of

m dor scap
i— m cuc
A

m oper

m procorhum
m dorhum

m anc scap med m supco r

m anc hum lat

m humantbr

Figure 13-31. Shoulder and pectoral girdle m procorhum

musculature of the salamander Salamandra
salamandra, redrawn from Francis (1934).
A. Superficial extensor muscles of the right m humantbr
shoulder and upper arm in dorsolateral view. m coracorad prop
B. Superficial flexor muscles of pectoral región
m supcor
and left upper arm in ventral aspect.
Abbreuiations: m anc coracoid = m. anconeus
coracoideus; m anc hum lat = m. anconeus
humeralis lateralis; m anc hum med = m. humerus
anconeus humeralis medius; m anc scap med =
m. anconeus scapularis medialis; m coracobrach
long = m coracobrachialis longus; m coracorad m anc coracoid
m pect
prop = m. coracoradialis proprius; m cuc = m coracobrach long
m. cucullaris; m dor scap = m dorsalis m anc coracoid
scapulae; m dorhum = m. dorsohumeralis; m
humantbr = m. humeroantibrachialis; m
oper = m. opercularis; m pect = m. pectoralis; m rect abdom sup
m procorhum = m. procoracohumeralis; m rect
abdom sup = m. rectus abdominis superficialis;
m supcor = m. supracoracoideus.
 Musculoskeletal System
fe scapula. The general function of this muscle is to dorsal facia, and its fibers converge to a superficial, ten- 339
the pectoral girdle to the axial column thereby dinous attachment with the head of the humerus. Con-
íorming an elastíc suspensión for the anterior end of the traction of this muscle pulís the upper arm backward. The
body. However, the m. thoraciscapularis is separable into m. latissimus dorsi is innervated by the dorsohumeralis
•me parís. The straight portion inserts on the dorsomedial netve which emerges from the anastomosis of S.Nn. 3
bortier of the suprascapula; contraction of this part de- and 4.
jresses the scapula and, as a consequence, expands the
•aer.tral portions of the girdle. An oblique portion inserts M. dorsalis scapulae
or áne posterodorsal angle of the suprascapula and re- The m. dorsalis scapulae (= m. deltoides of some au-
fcaos the scapula. The m. thoraciscapularis is innervated thors) is a fan-shaped muscle that arises from the dorso-
- E Nn. 2-4. lateral surface of the cartilaginous suprascapula (Fig.
Forelimb extensors and abductors.—Among the 13-31). Its fibers converge to a tendinous insertíon on
Hioulder muscles are three, the mm. dorsalis scapulae, the crista ventralis of the humerus. Contraction of this
zcssimus dorsi, and subscapularis, that act as forelimb muscle, which is innervated by S.N. 3, abducts the hu-
ecensors— that is, they are responsible for moving the merus.
rorr-.erus backward. M. subscapularis
The m. subscapularis arises from the dorsal surface of
M. latissimus dorsi the procoracoid and inserts on the humerus. It is inner-
The m. latissimus dorsi (= m. dorsohumeralis of Fran- vated by S.N. 3 and acts along with the m. latissimus
zs. 1934) is a triangular píate of muscle that is situated dorsi to extend or draw the upper arm backward toward
ne?ónd the shoulder (Fig. 13-31). It originales from the the flank.

B
IV

m ext brev dig

m intmetcarp

m ext lat dig IV

m abd &ext d¡g I m ext antbr &

carp uln
m ext antbr & carp rad Figure 13-32. Muscles of the right
forearm and hand of the salamander
Salamandra salamandra, redrawn
m ext antbr & carp uln from Francis (1934). A. Extensor
ext antbr & muscles of dorsal surface in
carp rad mfl antbr Etcarp rad superficial vieiv and B. deep view.
C. Flexor muscles of ventral surface
-m ext dig com in superficial view and D. deep view.
Abbreviations: m abd & ext dig I =
m. abductor et extensor digiti I;
m contra (cap long) = caput longum
of m. contrahentium; m contra dig =
m. contraríenles digitorum; m ext
antbr & carp rad = m. extensor
D antibrachii et carpí radialis; m ext
m fl brev prof antbr & carp uln = m. extensor
m intph antibrachii et carpí ulnaris; m ext
brev dig = m. extensor brevis digiti;
m contra dig m ext dig com = m. extensor
digitorum communis; m ext lat dig
m pron prof IV = m. extensor lateralis digiti IV;
m ext lat dig IV m fl acc lat = m. flexor accessorius
lateralis; m fl acc med = m. flexor
m fl brev sup m fl acc med accessorius medialis; m fl antbr &
m fl acc lat carp rad = m. flexor antibrachii et
m ext antbr & carpí radialis; m fl antbr & carp
m contra (cap long) carp rad uln = m. flexor antibrachii et carpí
ulnaris; m fl brev prof = m. flexor
m fl antbr & carp rad brevis profundus; m fl brev sup = m.
m fl antbr &carp uln flexor brevis superficialis; m fl prim
com = m. flexor primordialis
— m fl prim com— communis; m intmetcarp = m.
intermetacarpalis; m intph = m.
interphalangeus; m pron prof = m.
pronator profundus.
MORPHOLOGY
340 jVf. anconeus acoid cartilage. lis fan-shaped fibers converge to a tendor.
The major and proximal extensor of the forearm is the Ihal inserís along wilh Ihe m. pectoralis on Ihe posten::
m. anconeus ( = m. tríceps) which lies along the dorsal face of Ihe humerus. The m. supracoracoideus is inner-
surface of the humerus (Fig. 13-31). This muscle origi- valed by S.Nn. 2 and 3, and il is anlagonislic lo the dor-
nates from the humerus and the pectoral girdle via four sal exlensor, Ihe m. dorsalis scapulae, because Ihe rr.
heads which unite distally to insert on the olecranon process supracoracoideus adducls Ihe humerus, Ihereby drau.-
of the ulna. The muscle is innervated by S.N. 3 and it ing Ihe arm toward Ihe body, and flexes Ihe elbov.
acts to extend or straighten the elbow joint. joinl.
Distal forearm extensors.—Distal forearm extensors
include the mm. extensor digitorum communis, extensor M. coracobrachialis
anübrachii et carpi radialis, and extensor antibrachii et The m. coracobrachialis arises by lwo heads, both c:
carpi ulnaris, all of which arise from the humerus and are which origínale from Ihe ventral surface of Ihe coracoic.
innervated by branches derived from S.N. 3 or the anas- The m. coracobrachialis inserís along the posterior face
tomosis of S.Nn. 3 and 4 (Fig. 13-32). of Ihe humerus and flexes Ihe shoulder joinl, thereby
The m. extensor digitorum communis is the most su- drawing Ihe arm backward.
perficial and prominent of the three muscles. It sepárales
into four to six sepárate tendons which insert on the dor- M. humeroantibrachialis
sal surfaces of the digits, and acts to extend the wrist joint There is one major muscle responsible for flexión o:
and, therefore, the hand as a whole. The mm. extensor bending of Ihe elbow joinl. This is Ihe m. humeroanti-
antibrachii et carpi ulnaris and extensor antibrachii et carpi brachialis (= m. bíceps), which is innervated by branches
radialis act in tándem to extend the forearm by straight- of S.N. 4 (Fig. 13-31). The muscle arises from Ihe flexor
ening the elbow joint. The former muscle inserís on the side of Ihe humerus; ils fibers, which parallel Ihe hu-
distal end of the ulna, whereas the latter inserís on the merus, inserí on Ihe proximal end of Ihe radius.
distal end of the radius.
In additíon to the extensor muscles described above, Distal forearm flexors
Ihere are four more groups innervaled by branches of Dislal forearm flexors include Ihe mm. flexor antibra-
Ihe same spinal nerves that extend and roíale Ihe digils. chii el carpi radialis, flexor carpi ulnaris, flexor antibrachi:
They origínate from the wrisl and exlend lo Ihe meta- ulnaris, and flexor digitorum communis, which are sup-
carpals or phalanges. They are the mm. abductor and plied by branches of S.N. 4 (Fig. 13-32). Each of these
exlensor digiti primi, exlensores breves digitorum, and muscles orginates from the lateral epicondyle of Ihe hu-
exlensor laleralis digili quadrati. merus and inserís in Ihe áreas of Ihe lower forearm and
Forelimb flexora and extensors.—Four pectoral, or hand. The m. flexor antibrachii el carpi radialis insers
chesl, muscles are involved in Ihe ventral musculature along Ihe exlernal face of Ihe radius and the radíale,
thal acls as flexors of Ihe forelimb (Fig. 13-31); these are whereas the m. flexor antibrachii ulnaris inserís along the
the mm. pectoralis, procoracohumeralis, supracoracoi- ouler edge of Ihe ulna and Ihe m. flexor carpi ulnaris on
deus, and coracobrachialis. the lateral surface of Ihe ulnare. These three muscles flex
Ihe wrisl joinl, lending lo cióse Ihe angle belween Ihe
M. pectoralis forearm and Ihe hand. The m. flexor digitorum com-
The m. pectoralis is a superficial, fan-shaped muscle munis is a thin, fíat sheel of muscle Ihal arises from Ihe
that originales from Ihe fascia of Ihe m. reclus abdominis humerus; dislally, in the palm of the hand the muscle
and covers Ihe posterior región of Ihe breast. The fibers passes inlo a flal tendón Ihal divides inlo four parts anc
converge to a lendinous insertion on Ihe posterior surface passes along the digits lo inserí on the terminal pha-
of Ihe humerus along wilh Ihe m. lalissimus dorsi, an langes. This muscle is responsible for flexing the wrisl
extensor muscle. The muscle is innervated by branches and hand as a whole. There is a series of deep, ventrai
of S.Nn. 4 and 5, and acls to adducl Ihe arm, or draw it muscles Ihal are responsible for flexing Ihe wrisl and the
inward toward Ihe body and backward. digils, and for adducling Ihe digils. For further delails
aboul Ihese, see Francis (1934).
M. procoracohumeralis
The m. procoracohumeralis orginales from the dorsal Forelimb Movemcnt. As explained by K. Liem (1977).
surface of Ihe procoracoid cartilage and inserís near Ihe movemenls of Ihe forelimb can be subdivided inlo lwo
head of Ihe humerus. II is innervated by branches of locomolory phases—propulsive and recovery. The pro-
S.Nn. 2 and 3, and is anlagonisüc lo Ihe m. lalissimus pulsive phase consiste of backward movemenl of Ihe hu-
dorsi, because Ihe m. procoracohumeralis flexes Ihe merus accompanied by flexión of Ihe elbow joinl and
shoulder joinl Ihereby drawing Ihe upper arm forward. carpus. The relractíon of Ihe humerus is caused by con-
ftaction of Ihe mm. lalissimus dorsi, pectoralis, procora-
M. supracoracoideus cohumeralis, and coracobrachialis, which act on the
The m. supracoracoideus is superficial and lies anterior shoulder joinl. Concurrenlly, Ihe elbow and carpomela-
lo Ihe m. pectoralis. The muscle originales from Ihe cor- carpal joinls are flexed by the mm. humeroantibrachialis
 Musculoskeletal System
achii et carpi radialis, flexor carpi ulnaris, and recovery phase but toward the end of the phase, the 341
• . r.chii ulnaris. The contraction of these mus- m. extensor digitorum communis contraéis to extend the
•yff aoog with the flexor digitorum communis and other wrist and hand as a whole. The elbow joint never is
• of the digits, acts to straighten the arm and extended completely; however, a decrease in its angle of
pHB ÉK digits against the substrate. Thus, friction is in- flexión and a general stabilization of the joint is accom-
:. :he chance of backward slip diminished. In plished through the action of the forearm extensors, and
. the forelimb forms a weight-support column the mm. anconeus, extensor anübrachii et carpi radialis,
íts the propulsive forcé supplied by the hind- and extensor antibrachii et carpi ulnaris.
• - -. ground.
T^erecovery phase of the forelimb begins when the Pelvic Girdle Structure. The pelvic girdle of sala-
:• •-: ^::ted from the ground. The humerus is pro- manders consists of a ventral puboischiac píate and a
•: r.\d and upward by the contraction of the dorsal, club-shaped pair of ilia that are attached dorsally
: nz.is scapulae and procoracohumeralis. The el- to the sacral diapophyses of the sacral vertebra by fibrous
: : A'rist remain flexed during the first parí of the üssue (Fig. 13-33). Ventrally, the ilium of each half of the

fibular
con

femur-pubic lig
femur-ilial lig

Figure 13-33. Posterior

appendicular skeleton of Salamandra
salamandra, redrawn from Francis
(1934). A. Dorsal view of right foot.
B. Ventral view of right foot.
C. Extensor surface of right fémur.
D. Ventral aspect of ypsiloid
cartilage. E. Flexor surface of right
fémur. F. Pelvic girdle in
ventrolateral and G. dorsomedial (G)
aspeéis. Cartilage is in stippled
pattern. Abbreviations: con =
condyle; lig = ligament; p =
process; tar = tarsal.
MORPHOLOGY
342 pelvic girdle joins the ischium posteriorly and the pubis these respective muscle complexes in the forelimb. In the
anteriorly to form the acetabulum lateraily for the artic- hip joint, the fémur is capable of wide, elliptical excur-
ulation of the fémur. The ischia are represented by a pair sions, which are greater in the horizontal than in the ver-
of rounded ossifications in the posterior portion of the tical plañe. Movement of the knee and ankle joints is
puboischiac píate; the anterior cartilaginous part of the restricted for the most part to flexión and extensión, al-
píate is the pubic cartilage which is perforated by a small though some rotation takes place.
obturator foramen for the passage of the obturator nerve. Hindlimb extensors.—Extensión of the hip joint b
The halves of the girdle are united by a symphysis. All powered by one major derivativa of the dorsal muscu-
salamanders except the sirenids, proteids, amphiumids, lature and one derivative of the ventral musculature.
and plethodontids have an ypsiloid cartilage in associa-
üon with the pelvic girdle. This Y-shaped structure lies in M. iliofemoralis
the midline dorsal to the m. rectus abdominis and ante- The m. iliofemoralis is innervated by branches of S.Nn
rior to the puboischium with which it articúlales. The 16 and 17. It is the deepest of the thigh muscles, origin-
ypsiloid cartilage has been associated with hydrostatic ating on the posterolateral face of the ilium and the dorsa.
function of the lungs. By elevating the cartilage, the sal- (i.e., inner) face of the ischium and inserting along th=
amander is thought to compress the posterior end of the middle of the posterior surface of the fémur. The m.
body cavity and forcé air in the lungs forward, thereby iliofemoralis extends the hip joint and draws the thigh
causing the head to rise in the water. Conversely, when backward.
the ypsiloid cartilage is depressed, air is thought to move
posteriorly in the lungs, thereby reducing the buoyancy M. ischiofemoralis
of the head so that it tends to sink in the water. A derivative of the ventral musculature, the m. ischio-
femoralis extends the hip joint thereby pulling the fémur
Hindlimb Structure. Proximally, the fémur articú- backward. This short muscle arises from the inner s\¿¿
lales with the pelvic girdle by means of a ball-and-socket of the ischium and inserts on the posterior face of the
joint. The shank (or crus) consists of a pair of bones, the head of the fémur (Fig. 13-34). The muscle is innervatec
tibia and fíbula (Fig. 13-33). The mesopodial elements by branches of S.Nn. 16 and 17.
tend to be reduced through both loss and fusión and are
largely cartilaginous. Usually there are four metapodial Mm. iliotibialis, ilioflbularis,
elements (metatarsals) associated with the five digits with and ilioextensorius
a phalangeal formula of 1-2-3-3-2 (Fig. 13-33). Occa- Three dorsal muscles are responsible for extensión c:
sionally (e.g., plethodontids) the lengths of the digits are the knee (i.e., lower part of hindlirnb), and all are inner-
modified by reduction in the sizes of the phalangeal ele- vated by branches of S.Nn. 16 and 17 (Fig. 13-34). The
ments or by loss of a terminal element on Digit IV. A m. iliotibialis arises from two heads from the dorsolatera.
number of salamanders that otherwise have normal hind- surface of the ilium and passes superficially along the
limbs have lost the fifth (i.e., outer or postaxial) toe; among dorsal, extensor surface of the thigh and over the knee
these are Hynobius and Batrachuperus (hynobiids), Sal- to a tendinous insertion on the tibia. The m. iliofibular;
amandrina (salamandrid), Necturus (proteid), and Batra- arises from the lateral face of the ilium, posterior to the
choseps, Hemidacfylium, and some Eurycea (plethodon- origin of the m. iliotibialis, and extends along the posterc-
tids). dorsal border of the thigh to a tendinous insertion on the
proximal end of the fíbula. In conjunction with the m.
Musculature of Pelvic Girdle and Hindlimb. Un- iliotibialis, the m. ilioflbularis acts to extend, or straighten.
like the muscles of the forelimb and shoulder of sala- the knee joint and, therefore, extend the lower leg; how-
manders, those of the hindlirnb do not tend to spread ever, in combination with the ventral flexor, the m. pu-
out over the axial musculature (Fig. 13-34). The primary botibialis (see below), contraction of this muscle flexes
reason for this is that the pelvic girdle is anchored firmly the shank. Contraction of a third muscle, the m. ilioex-
to the axial column by way of a fibrous connection be- tensorius, also extends the knee joint, moving the shank
tween the ¡lia and the sacral vertebra; therefore, addi- forward. The m. ilioextensorius originales from the- tlíum.
tional suspensory muscular support is unnecessary. Given runs parallel with, and posterior to, the m. iliotibialis.
this fact, derivatives of axial musculature are not spe-
cialized for support of the pelvis and movement of the Mm. extensor digitorum communis,
upper part of the limb as they are in the forelimb. e. tarsi tibialis, and e. cruris tibialis
The hindlirnb musculature can be separated into two There are three primary dorsal extensor muscles that
general groups—those that are derivatives of dorsal or origínate from the lateral epicondyle of the fémur and
epaxial musculature, and those that are derivatives of extend beyond the knee; each is innervated by branches
ventral or hypaxial musculature. Generally, derivatives of of S.Nn. 16 and 17 (Fig. 13-34). The m. extensor digi-
the dorsal musculature are flexors, whereas ventral de- torum communis is the most superficial muscle. From its
rivatives are extensors, in contrast to the functions of origin, it spreads out into a thin, fan-shaped muscle that
 Musculoskeletal System
-m puboischfem 343
i—m ext iliotib

i-m ext crur tib

r-m ext dig com
m abd & ext dig I

Figure 13-34. Musculature of the

right hindlimb of the salamander
-m iliofib Salamandra salamandra, redrawn
m ext crur Star fib from Francis (1934). A. Superficial
IV extensor muscles in dorsal aspect.
•-ITI caudfem m ext brev dig- B. Superficial flexor muscles in
ocaud ventral view. C. Deep flexor muscles
in ventral aspect. Abbreviations: fas
plan = fascia plantaris; m abd dig
m puboischfem ext-| V = m. abductor digiti V; m abd &
m pubotib- ext dig I = m. abductor et extensor
digiti I; m caudfem = m.
caudalifemoralis; m caudpuboischtib
= m. caudalipuboischiotibialis; m
contra = caput longum of m.
contrahentium; m contra dig = m.
contrahentis digitorum; m ext brev
dig = m. extensor brevis digitorum;
m ext crur tib = m. extensor cruris
tibialis; m ext crur & tar fib = m.
extensor cruris et tarsi fibularis; m
ext dig com = m. extensor digitorum
m puboischtib- communis; m ext iliotib = m.
m caudpuboischtib m ischcd extensor iliotibialis; m ext tar tib =
fas plan—1 m. extensor tarsi tibialis; m femfib =
m pnm com—1 -m ischflex m caudfem m. femorofibularis; m fl acc lat = m.
flexor accessorius lateralis; m fl acc
m puboischfem int- -m pubifem med = m. flexor accesorius medialis;
m fl brev sup = m. flexor brevis
m ext tar tib-, i-m ext crur tib rm puboischfem
superficialis; m iliocaud = m.
m pron prof—-| r-m pubotib ext iliocaudalis; m iliofib = m.
m fl brev sup- iliofibularis; m intmettar = m
intermetatarsalis; m iph = m
interphalangeus; m ischcd = m.
ischiocaudalis; m ischfem = m.
ischiofemoralis; m ischflex = m.
ischioflexorius; m prim com = m.
primordialis communis; m pron
prof = m. pronator profundas; m
pubifem = m. pubifemoralis; m
puboischfem ext = m.
iph m pnm com—1 puboischiofemoralis externus; m
m puboischtib-1 puboischfem int = m.
m contra dig—1 m ischfem- puboischiofemoralis internus; m
m abd dig V—' m puboischtib- puboischtib = m. puboischiotibialis;
m fl acc Lm fl acc lat m pubotib = m. pubotibialis.

extends down the shank and onto the dorsum of the foot. a supine posiüon. The third muscle is the m. extensor
At the bases of the digits, nine tendons arise from this cruris tibialis, which inserís along the entire laíeral border
muscle; eight insert on either side of the bases of the of the fibia and extends to the tibíale and prehallux car-
metatarsals, whereas the ninth inserís on the lateral, or tilage, and extends the ankle joint.
fibulare, side of the first metatarsal. The extensor digi-
torum communis is the chief extensor of the foot. The Disto/ extensors
m. extensor tarsi tibialis is a small muscle that shares a The dislal, dorsal exíensors of íhe digiís are the mm.
common origin with, or arises cióse to, the extensor dig- exíensores digitorum breves. This complex is divisible
itorum communis. It is spindle-shaped and passes along into many muscles associaled wiíh íhe individual digiís
the m. extensor cruris tibialis to insert on the ventral sur- (see Francis, 1934, for explanatíon), buí is composed
face of the tibíale and prehallux cartilage. The primary primarily of superficial and deep sírata. The muscles gen-
action of the extensor tarsi tibialis is to turn the foot into erally arise from the íarsal elemenís and inserí by lendons
MORPHOLOGY
344 at the base of the terminal phalanx of each digit (Fig. Caudal muscles
13-34). Each tendón is attached to the other, more prox- There is a group of three tail muscles that arise from
imal phalanges by means of small, lateral slips at the the ventral surface of the fourth and fifth caudal verte-
interphalangeal joints. brae. One of these, the m. caudalifemoralis (Fig. 13-34).
Hindlimb flexors.—One derivative of the dorsal mus- inserts on the fémur and exerts a powerful backward pul
culature, the m. puboischiofemoralis internus, along with on the thigh while flexing the tail at the same time. Al-
several ventral muscles of the hip and thigh act chiefly though the two remaining muscles are associated witr
to flex the hip joint, adduct the fémur, and flex the knee the pelvic girdle and thigh musculature, their function ^
joint. limited to flexión of the tail. From its posterior origin, the
m. caudalipuboischiotibialis extends anterolaterally to in-
M. puboischiofemoralis sert by a fíat tendón into the posterior edge of the su-
The m. puboischiofemoralis internus is a large, pow- perficial ventral flexor, the m. puboischiotibialis. The m.
erful muscle (innervated by branches of S.Nn. 15-16 in ischiocaudalis passes forward from its origin between the
Salamandra) that arises from the entire dorsal side of the m. caudalipuboischiotibialis and the cloaca to insert o-.
pubis and parts of the ischium and ilium (Fig. 13-34). It the posterior border of the ilium.
bends around the anterior edge of the pubis and extends
along the anterior surface of the thigh to insert on the M. flexor primordialis communis
anterior end of the shaft of the fémur. Contracüon of this The primary flexor of the foot is the m. flexor primor-
muscle flexes the hip joint, rnoving the fémur forward. dialis communis that arises mainly from the lateral surface
The action of the m. puboischiofemoralis internus is an- of the fíbula; a few fibers origínate from the lateral ep:-
tagonistic to that of the m. iliofemoralis described above. condyle of the fémur. The course of this muscle parallels
The m. puboischiofemoralis externus arises from the the shank axis and passes into the plantar aponeurosis
ventral surface of the pelvic girdle at the anterior end of Distally, the aponeurosis divides into five tendons whicr
the pubis and inserís along the middle of the ventral extend along the flexor side of the digits and insert or.
surface of the fémur. This muscle is innervated by branches the proximal end of the terminal phalanx of each toe
of S.Nn. 15—17 and, on contraction, it serves as a flexor Each tendón of the flexor primordialis communis senes
of the hip joint moving the fémur forward. small, lateral slips to the proximal ends of the other phs-
langeal elements. In addition to flexing the entire focc
M. puboischiotibialis contraction of this muscle tends to turn the foot for-
The most superficial ventral muscle is the m. pubois- ward.
chiotibialis which arises lateral to the puboischiadic sym- There is a variety of accessory digital flexors (see Fran-
physis of the pelvic girdle and extends down the ventral cis, 1934) that act in concert with the flexor primordial
surface of the thigh to insert along the shaft of the tibia communis. These small muscles arise primarily from the
(Fig. 13-34). It bears a tough, fibrous conncction with distal ends of the tibia and fíbula and insert on the tarsals
the next muscle to be discussed, the m. pubotibialis, and and metatarsals; some extend between the tarsals ar.c
serves as the site of insertion of one of the tail muscles metatarsals. The chief action of these muscles is to abduc:
(m. caudalipuboischiotibialis). Acting alone, contraction the digits.
of this muscle flexes the knee, but acting in antagonism
to dorsal extensors, it causes flexión at the hip and
depression of the foot toward the substrate. Ai. flexor accessorius
Two additional muscles, the mm. flexor accessoriu;
M. pubotibialis lateralis and flexor accessorius medialis (Fig. 13-34), are
The m. pubotibialis has a tendinous origin from the involved in pronation of the foot. The lateral muscle arises
anteroventral edge of the pelvic girdle and extends along from the lateral edge of the fibulare and passes oblique;>
the ventrolateral border of the thigh to insert on the an- across the middle of the tarsus to insert on the plar.:;:
terior face of the proximal end of the tibia (Fig. 13-34). aponeurosis. The medial muscle originales from the distad
Its contraction adducts the hindlimb and tends to flex the two thirds of the fíbula along its ventromedial surfaée ar.c
knee. from the tarsal elements. It inserts on the dorsal surface
of the plantar aponeurosis.
M. ischioflexoris
The m. ischioflexoris is a strap-like muscle that origi- M. interosseus crurts
nales from the ventrolateral angle of the ischium just pos- The final muscle to be considered is the m. interosseus
terior to the origin of the m. puboischiotibialis (Fig. cruris, which is a thin sheet of muscle that joins the inner
13-34). The m. ischioflexoris passes along the poster- sides of the tibia and fíbula. It arises along the próxima-
oventral border of the thigh and inserts into the aponeu- surface of the fíbula, inserts on the distal surface of the
rosis of the m. flexor primordalis communis on the plan- tibia, and functions as an elastic ligament between the
tar surface of the foot. two bones.
 Musculoskeletal System
Hindlimb Movement. Movements of the hindlimb, chiofemoralis externus. Coincident flexión of the knee 345
ñs£ those of the forelimb, are divisible into propulsive and ankle joints is powered by contraction of the
3r.c recovery phases. According to K. Liem (1977), the m. ischioflexoris. Action of the m. flexor primordialis
• ve phase is initiated at the time the solé of the communis presses the foot and digits against the sub-
ixx contacts the substrate and consists of backward strate, preventing the foot from slipping backward. In the
mcvcment of the fémur (i.e., the thigh) accompanied by propulsive phase, the fémur acts as a driving lever that
fabon of the shank and foot. Retractíon of the thigh propels the body forward as it swings back in a horizontal
dáefiy results from contraction of the ventral, caudal plañe. The forcé is transmitted from the thigh to the ground
•úsele, the m. caudalifemoralis, in associatíon with two via the flexed limb, of which the foot and lower leg rep-
«entral thigh muscles, the mm. iliofemoralis and pubois- resent a staüonary pivot on which the fémur rotates.

prepollex
céntrale
radiale

cr lat

Figure 13-35. Anterior

appendicular skeleton of Rana
escalenta redrawn from Gaupp
(1896). A. Dorsum of right hand.
B. Venter of hand. C. Medial view of
right humerus. D. Dorsal view of
right radioulna. E. Lateral view of
right humerus. F. Pectoral girdle in
glenoid cav ventral view with scapula and
suprascapula deflected ventrally into
coracoid abdominal plañe. Stippled áreas are
epicoracoid cartilaginous. Abbreviations: cav —
cavity; cpl(s) = carpal(s); cr lat =
crista lateralis; cr med = crista
medialis; cr vent = crista ventralis;
lat epicon = lateral epicondyle;
tuber = tuberosity.
MORPHOLOGY
o4b jhe recovery phase begins as the foot rolls gradually short (i.e., one-third or less the length of the clavicle) anc
off the substrate. At this time the upper and lower por- proximally uncleft or unicapitate. Among more advancec
tions of the hindlimb are protracted forward as a unit anurans, the scapula is relatively longer and bicapitate.
through the combined action of several muscles. The The zonal área of the pectoral girdle can be definec
m. puboischiofemoralis acts on the thigh, whereas the as all those parts ventral and medial to the glenoid fossa£
mm. iliotibialis, ilioextensorius, iliofibularis, extensor tarsi (Fig. 13-35). These, in turn, are classified as prezona-
tibialis, and extensor cruris tibialis protract the shank. When zonal, and postzonal elements in an anterior to posterior
the hindlimb is protracted to a position slightly beyond a sequence. If present, the prezonal element is termed the
right angle to the body, the knee is flexed. The limb then omosternum (= episternum). Zonal components induce
is protracted further forward while the m. extensor digi- the clavicles (present in all anurans except some micro-
torum communis extends the foot. When the foot is placed hylids), coracoids, and the cartilaginous are that unites
on the substrate, another propulsive phase begins. the clavicle and coracoid of each half of the girdle in the
midline. The medial part of the cartilage is known as the
Anurans epicoracoid cartilage, whereas the anterolateral portior
Relative to that of primitive tetrapods and salamanders, that may be associated with the clavicle is termed the
the appendicular morphology of anurans is highly de- procoracoid cartilage. The división between these tv.:
rived and modified to provide for their saltatorial mode areas of cartilage in adults is arbitrary. The postzonal pzr.
of locomotion. Features of pectoral girdle morphology oí the pectoral girdle is the sternum, which is subdividec
have been used in the major classification of anurans in some frogs into a mesosternum proximally and a »-
since Cope (1864, 1865); consequently, many system- phisternum distally.
atic papers include descriptions of the pectoral girdle. Arcifery and flrmistemy.—Basically, there are tu:
Similarly, because the ilia of the pelvic girdle frequently kinds of pectoral girdles in anurans depending on the
are found as fossils, there exists considerable miscella- relationship of the zonal elements (Griffiths, 1959a). The
neous information on this unit. The most important most widespread pattern is arcifery in which the epiccr-
morphological literature relating to the appendicular skel- acoid cartilages are elaborated into posteriorly directe:
eton was summarized by Trueb (1973). Significant con- epicoracoid horns (Fig. 13-36). The latter articúlate wir
tributions include those by S. Emerson (1983, 1984) on the sternum by means of grooves, pouches or fossae ir.
the pectoral girdle and T. Creen (1931), Whiting (1961), the dorsal surface of the sternum and provide a surface
S. Emerson (1979, 1982), and S. Emerson and De Jongh for the insertion of a pair of muscles derived from the rr.
(1980) on functional aspects of the pelvic girdle. Ander- rectus abdominis. Most arciferal anurans also are char-
sen (1978) surveyed the carpus and tarsus of anurans, acterized by fusión of the epicoracoid cartilages in the
and Alberch and Cale (1985) described digital reduction interclavicle región. Posterior to the clavicles, the epicor-
in amphibians. acoids usually are free and overlapping.
The firmisternal girdle characteristic of ranids, micrc-
Pectoral Girdle Structure. In contrast to salaman- hylids, and dendrobatids lacks epicoracoidal horns (F:c
ders, most anurans retain two dermal bones in their pec- 13-36). The sternum is fused to the pectoral arch. anc
toral girdles—the clavicle and cleithrum (Fig. 13-35). En- the epicoracoidal cartilages of each half of the girdle are
dochondral components include the scapula and coracoid. fused to one another. The midzonal length of the gir¿£
For purposes of discussion, it is easiest to consider each is shorter than that of an arciferal girdle, but pre- and
half of the pectoral girdle to consist of two áreas—the postzonal elements tend to be much longer.
scapula-suprascapula área above the glenoid fossa and A few anurans have pectoral girdles that are modifíed
the zonal área below it (Fig. 13-35). The dorsal half of to produce so-called pseudofirmisternal or pseudoarc-
the glenoid fossa is formed by the proximal end of the feral conditions from arciferal and firmisternal girdles. re-
scapula. Distally, the scapula is expended and articulates spectively. For example, in some bufonid genera (e.g..
with the bony base of the suprascapula. The supra- Atelopus, Oreophrynella, Dendrophryniscus), and lep-
scapula varíes from a blade shape to a fan shape. At least todactylids (e.g., Sminthillus, Geobatrachus, Phrynopus
a part of the leading edge ¡s bony, and this ossification the fusión of the epicoracoid cartilages in the-región of
represents the cleithrum. Ossification from the cleithrum the epicoracoid bridge is extended posteriorly. Thus. the
invades the suprascapular cartilage to varying degrees in cartilages no longer overlap freely, and functionally. a
different species of anurans; thus, ossification of the su- partially firmisternal condition is created. The pipid frog
prascapula might be limited to the anterior and ventral Hymenochims represents an extreme of pseudofirmis-
margins, or as is more commonly the case, one-third to terny in which the epicoracoid cartilages are fused
two-thirds of the blade may be ossified. In some hyper- throughout their lengths so that no movement of one
ossified frogs (e.g., Brachycephalus) the entire blade is half the girdle on the other is possible. Pseudoarcifery is
ossified (Fig. 13-36). The scapulae of primitive anurans known to occur only in a few species of ranids and the
(e.g., leiopelmatids, discoglossids, and pipids) tend to be sooglossids in which the epicoracoid cartilages are partly
 Musculoskeletal System
347

Figure 13-36. Diagrammatic ventral views of pectoral girdles of anurans. Scapulae and suprascapulae are
deflected ventrally into abdominal plañe. Cartilaginous áreas are stippled. A. Brachycephalus ephippium.
B. Kaloula pulchra. C. Bufo coccifer. D. Xenopus laevis. E. Scaphiopus hammondü. F. Alytes obstetricans.
G. Rana rugulosa. H. Rhinoderma daruiini. I. Ascaphus truei.
MORPHOLOGY
«48 free and overlapping; however, the epicoracoids are fused the radio-ulna. These are assumed to be the radíale (per-
to one another and the sternum posteromedially. haps fused with one of the céntrale series) preaxially anc
Prezonal structure.—The occurrence of prezonal ele- the fused intermedium and ulnare postaxially. Distal to
ments is irregular. Omosterna are usually present in fir- these two large elements are the prepollex (preaxial) anc
misternal anurans (Fig. 13-36). In its simplest state, the three centrales, the homologies of which are uncertain.
omosternum is a simple disc of cartilage that lies anterior Two small distal carpáis lie between the centrales and the
to the precoracoid bridge or the medial articulation of the series of four metacarpals. All anurans have four digis
clavicles. In some anurans (ranids especially), the omo- on the hand, and the normal phalangeal formula is 2-2-
sternum is elaborated into a long style with a terminal 3-3 (Digits I-IV, respectively). Reduction in the lengths
cartilaginous disc, and the style may be ossified. Arciferal of the phalanges (e.g., some species of the bufonid genuf
anurans frequently lack omosterna, and when present, Rhamphophryne, and the brachycephalids) or loss of a
this prezonal element usually is small. phalangeal element (e.g. some Atelopus) can result in
Postzona/ structure.—All anurans except Rhinophry- one or more shortened digits, although all anurans reta;.-,
nus and the brachycephalids have a sternum. The ster- at least the vestiges of four digits so far as is knour.
num has a variety of shapes (Fig. 13-36). Among firmi- Several groups of frogs—the hylids, centrolenids, hyper-
sternal anurans, it tends to be long (except in microhylids oliids, rhacophorids, pseudids, mantelline ranids, anc
with reduced girdles) and to be elaborated into an ossi- phrynomerine microhylids—are characterized by the
fied stylus (mesosternum) with an expanded cartilaginous presence of an additional element, the intercalary cart-
end (xiphistemum). The majority of arciferal anurans have lage or bone, between the penultimate and ultímate pha-
a broad, ovoid sternum that is proportionately shorter langes. Among leptodactylids, bufonids, hyperoliids. hy-
than that of firmisternal anurans. By comparison with all lids, centrolenids, and microhylids, the terminal or ultímate
other anurans, pipids of the genus Pipa especially, have phalanges frequently are modified into a variety of dif-
the largest sterna. In these frogs, the sternum covers most ieren! shapes.
of the abdominal región and is flanked anterolaterally by
the epicoracoid cartilages that have expanded postero- Forelimb Movement. Myologically, the pectoral re-
lateral to the coracoid bones. Because the sternum serves gión of anurans is highly modified and variable in com-
as a site of muscle attachments, it would seem that this parison with the generalized pattern characteristic of mos:
structural variation must have some funcüonal signifi- salamanders. The modification of the anterior append-
cance. But this, along with any functional differences that cular skeleton from a more generalized scheme obviousiy
might exist between the arciferal and firmisternal condi- is associated with the saltatorial habits of anurans. The
tions, is undetermined as yet. mechanics of the hindlimb have been analyzed by Gar.s
One anuran genus, Leiopelma, has so-called abdom- (1961) and Calow and R. Alexander (1973), but aside
inal or inscripüonal ribs that lie in the myosepta of the from S. Emerson's (1984) paper on some mechanica]
ventral trunk musculature, the m. rectus abdominis; these properties of arciferal and firmisternal girdles, nothing
are similar to structures that are found in the proteid specific is known about the role of the pectoral girdle and
salamander Necturus. There are three pairs of cartilagi- forelimbs in anuran locomotion. Based on personal ob-
nous elements posterior to the sternal horns. The pos- servatíons and Gans's (1961) stop-frame photographs of
terior two pairs may or may not be united medially; the ñaña caíesbeiana jumping, it is evident that the forelimb
halves of the anterior pair are fused medially and may of anurans is positioned differently than that of salaman-
be united synchondroücally with the sternum. According ders and fulfills a different functional role in locomotion.
to de Vos (1938), the ribs may be serially homologous At rest, the shoulder joint tends to be extended with the
~~-wjth the posterior horns of the sternum, but they are not upper arm lying against the flank raher than held at a
associated in any way with the ribs which are of dermal right angle to the body as it is in salamanders. The elbow
origin. joint is flexed and the forearm directed in an anterome-
dial direction rather than directly forward. Thus, the en-
Forelimb Structure. The proximal, or propodial, ele- tire lower arm and hand are rotated inward toward the
ment of the anuran forelimb ¡s the humerus (Fig. 13-35), center of the body. As the animal thrusts itself forward
which in males frequently is modified by the proliferation in a leap, it probably rolls off the palmar surface of the
of large crests for the attachment of hypertrophied mus- hand while straightening the elbow and wrist joints. Thus.
culature (Fig. 3-9). The radius and ulna are fused to form the forelimb lies parallel to the body for máximum
the compound epipodial bone—the radio-ulna. Although streamlining. After full thrust has been developed from
there may be as many as 12 mesopodial elements, there the hindlimbs, the forelimb is flexed at the elbow, and
is great variation in their number and configuration in the upper arm is pulled as far forward as possible. Sub-
anurans, and a tendency toward loss and fusión. The sequent flexión of the wrist allows the animal to land on
following description is based on the leiopelmatid Asca- its hands, the forcé of landing presumably being ab-
phus truel There are two large elements associated with sorbed by the pectoral girdle.
 Musculoskeletal System
ÜMSculature of Pectoral Girdle and Forelimb. girdle. Thus, it is difficult to present a generalized descrip- 349
• - - ¿iííerences in locomotion and the structure of tion. Among the most useful descriptions available are
tic pectoral girdle between salamanders and anurans, it those of Gaupp (1896) for ñaña esculenta, Ritland (1955)
s -oí surprising that anuran pectoral musculature is quite for Ascaphus trueí, T. C. Burton (1983a, 1983b) for mi-
dberent Moreover, the marked variability of pectoral crohylids, M. Davies and T. C. Burton (1982) for Rheo-
i structure in anurans is paralleled by an equivalent batrachus silus, S. Liem (1970) for rhacophorids and hy-
.-.: of variatíon in the muscles associated with the peroliids, and Grobbelar (1924) forXenopus laevis. De

m lev post long m dep mand

m pter m dor scap
m lat dor

fascia dor

m obl ext

m pect

m anc
m coracorad

m pter m lev post long

m lev scap sup
suprascapula
•m lev scap inf

m serr inf
m lev post long m cuc

m delt
m dor scap cap scap]
m anc Figure 13-37. Shoulder girdle musculature of
cap lat/ Rana esculenta redrawn from Gaupp (1896).
m lat dor
A. Superficial lateral view. B. Deep lateral view.
m rhomb ant C. Medial view of inner side of right side.
m rhomb post Abbreviations: cap lat = caput laterale of m.
m lev scap sup anconeus; cap scap = caput scapulare of m.
m serr sup anconeus; fascia dor = fascia dorsalis; m anc =
m serr med
suprascapula m. anconeus; m coracorad = m. coracoradialis;
m corbrach brev = m. coracobrachialis brevis;
m interscap m corbrach long = m. coracobrachialis longus;
m lev scap ¡nf m cuc = m. cucullaris; m delt = m. deltoideus;
m cuc
m obl ext (p scap) m dep mand = m. depressor mandibulae; m dor
m lev scap inf scap = m. dorsalis scapulae; m interscap = m.
m serr inf interscapularis; m lat dor = m. latissimus dorsi;
m delt m lev post long = m. levator mandibulae
m anc posterior longus; m lev scap inf = m. levator
scapulae inferior; m lev scap sup = m. levator
m corbrach long scapulae superior; m obl ext = m. obliquus
externus; m omohyd = m. omohyoideus; m
pect = m. pectoralis; m. pterygoideus; m rhomb
í-m coracorad ant = m. rhomboideus anterior; m rhomb post
= m. rhomboideus posterior; m serr inf = m.
m corbrach brev serratus inferior; m serr med = m. serratus
m coracorad medius; m serr sup = m. serratus superior; p
epistern = pars episternalis of m. deltoideus; p
o epicor- m delt scap = pars scapularis of m. deltoideus; p
m pect
Í p abdom
p stern
p episternf epicor = portio epicoracoidea of m. pectoralis; p
stern = portio sternalis of m. pectoralis.
MORPHOLOGY
350 Villiers (1922) produced a monograph that concentrated homologue in salamanders ¡s the m. cucullaris, which ¡s
primarily on the structure and development of the breasí- similarly innervated in both groups by C.N. XI (acces-
shoulder apparatus in Bambino uariegata, and E. Jones sory). From its origin on the prootic and the otic ramus
(1933) and Hsaio (1933-1934) provided comparative of the squamosal, the m. cucullaris extends posteroven-
studies of the pectoral regions of some anurans. There is trally to insert on the anterior border of the suprascapula
an appalling lack of concordance in the ñames applied It lies anterior and external to the m. levator scapulae
to various pectoral muscles. Because Gaupp's (1896) de- inferior. Contraction of this muscle depresses the head
scriptions are the most thorough and well documented, unless the head is immobilized by contraction of trunk
his nomenclature is adopted here, and unless otherwise musculature that attaches to the posterior end of the skul
stated, the following descriptions are based on Rana es- in which case the muscle pulís the suprascapula forward
culenta.
As in salamanders, the muscles of the anuran shoulder
and forelimb are separable into three groups—muscles M. rhomboideus posterior and serratas
that chiefly are suspensory in function, and those that There are four extrinsic muscles in anurans that sus-
extend and flex the forelimb. A fourth category that exists pend the pectoral girdle from the axial column and gen-
in anurans are intrinsic muscles that move one part of erally are antagonistic in action to the extrinsic muscles
the pectoral girdle with respect to another. arising from the skull (Fig. 13-37). This group of muscles
Suspensory muse/es of girdle.—The extrinsic sus- probably is homologous with the m. thoraciscapularis oí
pensory muscles are of two types—those that arise in salamanders. These muscles lie deep to the mm. latiss-
association with the vertebral column or the axial mus- mus dorsi and dorsalis scapulae (described below). Th=
culature and insert on the suprascapula, and those that two most posterior members of the series are the mra
arise from the posterior part of the skull and ¿xíend to rhomboideus posterior and serratus superior, both of whicr.
the suprascapula (Fig. 13-37). are innervated by branches of S.N. 3. The m. rhomboi-
deus posterior is dorsal in position and derived from the
M. rhomboideus anterior epaxial musculature. From its broad origin from the
The m. rhomboideus anterior ¡s a thin, broad, rhom- transverso process of Presacral IV, the muscle fibers con-
boidal muscle that is innervated by S.N. 3 and originates verge as the m. rhomboideus posterior extends anterior;.
from the posterior part of the frontoparietal bone and the to insert on the dorsomedial surface of the suprascapula
anterior part of the dorsal fascia. It is superficial in position Contraction of this muscle pulís the suprascapula back-
and extends posteriorly from the skull to insert on the ward. The m. serratus superior originates from the trans-
ventral surface of the anteromedial córner of the supra- verse process of Presacral IV distal to the origin of tr.€
scapula. Contraction of the rhomboideus anterior pulís m. rhomboideus posterior. This muscle extends ante-
the suprascapula forward. The muscle is enlarged in many riorly to insert on the dorsomedial surface of the supra-
species of Bufo and arises from the dorsal surface of the scapula beneath the point of insertion of the m. rhom-
prootic and the posteromedial part of the squamosal, as boideus posterior. The m. serratus superior retraéis the
well as the frontoparietal. suprascapula ¡n a posterolateral direction. The two re-
maining members of this series of dorsal suspensory mus-
Mm. levator scapulae and opercularis cles are the mm. serratus medius and serratus inferior
The levator scapulae complex is composed of three the former is innervated by S.N. 3, whereas the latter is
muscles that origínate from the prootic-exoccipital región innervated by S.N. 4. The m. serratus medius arises frorr.
of the skull and insert on the medial side of the supra- the transverse process of Presacral III and extends for-
scapula (Fig. 13-37). The m. levator scapulae superior ward to insert on the central, medial surface of the su-
arises from the lateral part of the oüc capsule and is in- prascapula. Contraction of this muscle pulís the supra-
nervated by S.Nn. 2 and 3. A dorsal derivative of this scapula in a lateral direction. The m. serratus inferior
muscle, the m. opercularis (see discussion of neurocranial arises from two heads. The posterior head is associatec
head musculature above), extends between the oper- with the transverse process and cartilaginous epiphysis oí
culum and the suprascapula in all anurans except pipids. Presacral IV, whereas the anterior head is associated witr.
The m. levator scapulae inferior has a broad origin from these parís of Presacral III. From its origins, the muscle
the prootic and exoccipital bones. The inferior muscle is gradually decreases in size as it extends anteriorly and
innervated by S.N. 2 and inserís on the posteroventral venfrolaíerally ío inserí on íhe medial surface of íhe su-
córner of the suprascapula, whereas the superior portion prascapula near íhe posferovenfral edge of íhis element
inserís on the anterodorsal córner. Both muscles protrací The m. serraíus inferior draws íhe ventral portion of íhe
fhe suprascapula. suprascapula posleromedially.
Forelimb extensors and adductors, and intrinsic
M. cucullaris pectoral muscles.—Forelimb exíension is powered by
The only muscle extending between the skull and the two shoulder muscles and a variety of distal muscles (Figs.
pectoral girdle in anurans for which there is an obvious 13-37, 13-38). Inírinsic pectoral muscles also are consid-
 Musculoskeletal System
i-m ti antbr lat prof 351
[~m fl antbr lat sup rm ext carp rad B
m abd ind long-
m coracorad r m abd ind long
E : brev sup- hum ev sup
IV I

prepollex-
mext md brev med-1
m abd ¡nd brev dor-l um ti carp rad -m ext dig com long
m palm long-1 -m fl carp uln Lm ext carp uln

D
m lumb brev
m lumb long

~i abd ¡nd long -tendon-

m lumb brev
ext brev sup

m ext ¡nd brev

m abd ind brev dor m_abd md long m abd primdiglV- m opp ind
m f l sup prop
m ext carp rad
m abd sec dig IV m add poli
m abd ind long m abd poli
m f I carp rad
m epicondcub
m palm prof
m fl antbr lat prof m epitrochcub
m coracorad m ext carp uln
m palm long

m ext carp rad

Figure 13-38. Distal forelimb musties of Rana escalenta, redrawn from Gaupp (1896). A. Medial aspect of
right hand and forearm. B. Lateral aspect of right hand and forearm. C. Dorsal surface of right hand and
forearm with superficial muscles removed. D. Ventral aspect of right hand and forearm. Abbreviations:
aponeur palm = aponeurosis palmaris; hum = humeras; m abd ind brev dor = m. abductor indicis brevis
dorsalis; m abd ind long = m. abductor indicis longus; m abd poli = m. abductor pollicis; m abd prim dig
IV = m. abductor prinius digiti IV; m abd sec dig IV = m. abductor secundus digiti IV; m add poli =
m. adductor pollicis; m coracorad = m. coracoradialis; m epicondcub = m. epicondylocubitalis; m
epitrochcub = m. epitrochleocubitalis; m ext brev med = m. extensor brevis medius; m ext brev prof = m.
extensor brevis profundus; m ext brev sup = m. extensor brevis superficialis; m ext carp rad = m. extensor
carpí radialis; m ext carp uln = m. extensor carpí ulnaris; m ext dig com long = m. extensor digitorum
communis longus; m ext ind brev = m. extensor indicis brevis; m ext ind brev med = m. extensor indicis
brevis medius; m fl antbr lat prof = m. flexor antibrachii lateralis profuncus; m fl antbr lat sup = flexor
antibrachü lateralis superficialis; m fl carp rad = m. flexor carpí radialis; m fl carp uln = m. flexor carpí
ulnaris; m fl sup prop = m. flexor superficialis proprius; m iph = m. interphalangealis; m lumb brev = m.
lumbricalis brevis; m lumb long = m. lumbricalis longus; m opp ind = m. opponens ¡ndicis; m palm long =
m. palmaris longus; m palm prof = m. palmaris profundus.
MORPHOLOGY
352 ered here, allhough they do not affect extensión of the medial surface of the humerus, and the ouler head from
forelimb directly. íhe lateral surface of íhe humerus. The fibers of Ihese
Ihree heads unile to form a robusl muscle Ihal covers íhe
Mm. latíssimus dorsi and dorsalis scapulae upper, inner, and ouler surfaces of íhe humerus and con-
These shoulder muscles are ¡nnervaíed by a branches verge on a tendón thal inserís oñ íhe proximal end of
of S.N. 3 and probably are homologous wilh íhe muscles íhe olecranon process of íhe radio-ulna. On conlractíon.
of íhe same ñames in salamanders. In mosl anurans íhe Ihis muscle straighlens íhe elbow, Ihereby extending íhe
m. laüssimus dorsi is superficial, íhin, and triangular and forearm.
arises from íhe ventral surface of íhe dorsal fascia; how-
ever, in some species of Bufo íhe muscle is narrow and Dista/ forearm extensors
ihick and arises from the cartílaginous epiphysis of the Dislal forearm extensors include íhe mm. exlensor carpí
transverse process of Presacral IV. lis fibers converge lo radialis, exlensor carpi ulnaris, epicondylocubitalis, epi-
a flal tendón Ihal inserís on íhe delloid crest (= crista Irochleocubilalis, exlensor digilorum communis longus.
ventralis) of íhe humerus. Conlraclion of íhe m. latissi- and abductor indicis longus (Fig. 13-38). Each of Ihese
mus dorsi exlends íhe shoulder joinl by pulling íhe upper muscles lakes ils origin, al leasl in part, from the latera!
arm backward. epicondyle of the humerus.
The m. dorsalis scapulae lies anterior lo íhe m. latís- The m. extensor carpi radialis arises by two heads. The
simus dorsi; il arises from íhe ouler (i.e., lateral) surface superior head originales from íhe lateral cresl of íhe hu-
of íhe suprascapula. From ils broad origin, íhe muscle merus, whereas íhe more dislal head arises from íhe lat-
converges inlo a flal tendón Ihal uniles wilh íhe tendón eral epicondyle of íhe humerus and íhe elbow joinl. Al-
of the m. latíssimus dorsi to inserí on íhe delloid crest of lhough the two heads are separaled Ihroughoul íhe greater
íhe humerus. The primary aclion of íhe m. dorsalis scap- part of their lenglhs, they unite dislally to cross the radio-
ulae is lo adducl, or raise, íhe humerus. In conjunclion ulna and inserí on íhe carpáis. The m. exlensor carp:
wilh íhe m. latissimus dorsi, Ihis muscle acls lo circum- radialis exlends íhe wrisl in a dorsal direclion.
ducl íhe humerus dorsally and backward. The m. extensor carpi ulnaris is a narrow muscle tha:
originales from the lateral epicondyle of íhe humerus.
Mm. interscapularís and sternoepicoracoideus exlends down íhe forearm, and inserís on íhe ouler sur-
There are lwo inlrinsic muscles associaled wilh íhe face of íhe carpus; contraclion of Ihis muscle exlends the
pectoral girdle in anurans—the mm. interscapularis and wrist joinl.
sternoepicoracoideus (= m. sternocoracoideus of some The m. epicondylocubilalis arises by lwo heads; one
aulhors). The m. interscapularis arises from íhe venrro- is localed on íhe lateral epicondyle of íhe humerus, whereas
medial surface of íhe suprascapula and exlends venlro- íhe olher is on íhe medial epicondyle. This muscle unites
medially lo inserí on the ventral surface of íhe scapula. medially with íhe m. epilrochleocubilalis, which arises
Il is innervated by a branch of C.N. X (vagus). Contrac- from íhe medial epicondyle, lo form a pinnale muscle
tion of Ihis muscle closes íhe angle belween íhe supra- Ihat extends dislally lo cover íhe olecranon process oí
scapula and íhe scapula. Allhough all anurans possess the radio-ulna and inserí on the dorsal border of the ulnar
Ihis muscle, il vanes in size and configuration. Il is bifúr- portíon of the radio-ulna. The muscle acls lo roíale íhe
cate in discoglossids, bul single in mosl olher anurans, forearm medially.
and varíes from large in bufonids lo small in ranids. The The m. exlensor digilorum communis longus lies on
second inlrinsic muscle, íhe m. sternoepicoracoideus, is the outer border of íhe forearm. Il originales from the
found only in discoglossids and Leiopelma. Il is inner- lateral epicondyle of íhe humerus and passes down the
vated by S.N. 3 and arises from íhe anterior border of forearm inlo an aponeurosis on íhe dorsum of íhe hand
íhe dislal parí of íhe slernal horn. From Iheir broad origin, The aponeurosis is continuous wilh lendons of íhe
íhe muscle fibers converge lo a narrow tendón Ihat in- m. extensor brevis digitorum that inserí on íhe phalangea!
serís anleromedially on íhe dorsal surface of íhe epicor- elemente; Ihus, íhe muscle is an exlensor of íhe wrisl and
acoid cartílage near ils posterior margin. The m. sternoe- Digils II-IV. The superior head of íhe m. abductor indicis
picoracoideus is Ihoughl lo be derived from íhe m. reclus longus has a common origin wilh íhe m. extensor digi-
abdominis. Ils functíon is unknown. torum communis longus, whereas ils lower head arises
from íhe lateral surface of íhe radio-ulna. The muscle
M. anconeus fibers unite lo exlend obliquely down and across íhe ra-
The major extensor of the elbow joint is íhe m. an- dio-ulna and inserí on Melacarpal I. Contraclion of Ihis
coneus which lies along íhe dorsal surface of íhe upper muscle extends the wrist and abducls the first, or inner.
arm. This muscle, along with all the other forearm ex- digit.
lensors, is innervated by branches of S.N. 2. The anco- In addition lo íhe exlensor muscles described above.
neus bears Ihree heads, íhe longest of which originales there is a multiplicity of muscles Ihat act lo extend and
from íhe posterior border of íhe scapula al the upper abduct the digits. The primary muscle is íhe m. extensor
border of the glenoid cavity where it is atlached lo íhe digilorum communis brevis Ihat arises from the wrisl and
joinl capsule. The inner head arises from íhe proximal, inserte on the terminal phalanx of Digits II-IV. Smaller
 Musculoskeletal System
abductors and extensors are associated with each sepa- insert on the deltoid crest of the humerus. Contraction 353
ras digit Gaupp (1896), S. Liem (1970), Andersen of the m. pectoralis adducts the upper arm downward.
1978). and T. C. Burlón (1983a) provided detailed de-
srtpnons of these muscles. Mm. coracobrachialis longus and brevis
Forelimb flexors and adductors.—Five pectoral mus- The two deep muscles, the mm. coracobrachialis lon-
des are involved in the ventral musculature that acts as gus and brevis, are innervated by branches of S.N. 3.
iexors of the shoulder and elbow joints (Fig. 13-37). The The m. coracobrachialis longus is a long, narrow muscle
JOST superficial of these are the mm. pectoralis, cora- that arises from the dorsal surface of the coracoid near
roradialis, and deltoideus. The mm. coracobrachialis lon- the sternum and extends laterally to insert on the middle
us and coracobrachialis brevis lie deep to these muscles. of the humerus. The m. coracobrachialis brevis arises
from the dorsal surface of the coracoid and scapula and
M. deltoideus inserts on the deltoid crest of the humerus. Contraction
The m. deltoideus (not homologous with the muscle of these two muscles pulís the arm posteroventrally;
oí the same ñame applied by some authors to the therefore, they are antagonistic to the m. deltoideus.
T- dorsalis scapulae of salamanders) is the most anterior
y. the three superficial muscles, and is innervated by Varíation in ventral pectoral musculature
rranches of S.N. 3.The m. deltoideus is composed of Given the great amount of variation in the structure of
Three parte—the partes episternalis, clavicularis, and the ventral parts of the pectoral girdle among anurans,
scapularis. The pars episternalis arises from the lateral one would anticípate correlative variation in the ventral
border of the omosternum and inserís on the distal por- pectoral musculature. Hsiao (1933-1934) and E. Jones
tón of the humerus. The pars clavicularis is a small mus- (1933) demonstrated that the mm. deltoideus, pectoralis,
z.z that originales from the lateral end of the ventral sur- and coracoradialis are the most variable. In anurans hav-
áce of the clavicle. This muscle unites with the third part ing a small omosternum or lacking this prezonal element,
;:' the m. deltoideus, the pars scapularis, to insert on the the origins of the anterior components of the mm. del-
áeltoid crest of the humerus. The pars scapularis arises toideus and pectoralis tend to be narrowed and shifted
rom the lateral end of the clavicle, the precoracoid car- posteriorly, and in some cases (e.g., some microhylids)
iage, and the anterior and ventral surfaces of the scap- these muscles may fuse. The clavicular portion of the
uia. Contraction of the various parts of the m. deltoideus, m. deltoideus is absent in many microhylids. The cla-
íexes the shoulder joint by pulling the humerus forward. vicular portion of the m. coracoradialis varíes with respect
to its attachment to the clavicle, and with reduction of
M. coracoradialis this element, the origin of the muscle may shift posteriorly
The m. coracoradialis lies posterior to the m. deltoi- to the procoracoid cartilage. In general, there is less var-
deus. It is a broad, fan-shaped muscle that overlies part iation in the posterior muscles, although the portio ster-
of the m. deltoideus anteriorly, and is partially covered nalis of the m. pectoralis tends to diminish in size in as-
posteriorly by the anterior part of the m. pectoralis. The sociation with smaller sterna, and in some microhylids
m. coracoradialis has a broad origin from the omoster- the m. pectoralis portio abdominalis is divided into medial
num and epicoracoid cartilage. The fibers converge lat- and lateral parts.
erally to a tendón that inserts on the proximal end of the
radio-ulna. This muscle, which is innervated by S.N. 3, Distal forearm flexors
is a powerful flexor of the elbow joint and, therefore, is The distal forearm flexors are complex; for conven-
antagonistic to the acüon of the m. anconeus. ience, they are broken into two groups—those that lie on
the medial surface of the forearm and those that lie on
M. pectoralis the lateral surface (Fig. 13-38). All are innervated by
The last and most posterior of the three superficial branches of S.N. 2.
pectoral muscles is the m. pectoralis which is composed The m. flexor carpi radialis is a superficial muscle that
of three parts and innervated by branches of S.Nn. 2 and takes a broad origin from the inner border of the humerus
3. The most anterior section is the portio epicoracoidea above the medial condyle. The fibers of this muscle con-
which has a broad origin from the epicoracoid cartilage verge distally on the forearm and insert on the carpus.
and overlies the posterior part of the m. coracoradialis. The m. flexor carpi ulnaris lies along the inner side of the
The fibers of this part of the m. pectoralis converge lat- m. flexor carpi radialis. The muscle originales from the
erally to a tendón that inserts on the deltoid crest of the median condyle of the humerus, and like the m. flexor
humerus. The portio sternalis arises from the sternum carpi radialis, it inserts on the carpus. Together, these
posterior to the portio epicoracoidea; its fibers converge two muscles serve as the main flexors of the hand. Typ-
anterolaterally and insert into the groove beside the del- ically, the m. flexor carpi radialis is better developed in
toid crest of the humerus. The most posterior and largest males than in females owing to the use of the forearm in
part of the m. pectoralis is the portio abdominalis. This males to grasp the female during amplexus. The third
muscle is derived from the m. rectus abdominis. From its superficial muscle of the medial side is the m. palmaris
broad, posterior origin, the muscle extends anteriorly to longus. This muscle arises from the medial epicondyle of
MORPHOLOGY
354 the humerus and the medial surface of the elbow joint. along the distal third of the ulna and extends around the
It extends down the forearm and passes into the trian- wrist and inserts on the ulnare. Contraction of this muscle
gular palmar aponeurosis. Tendons arise from the distal flexes the wrist thereby pulling the hand downward.
margin of the aponeurosis of the m. palmaris longus and On the lateral side of the forearm, the m. flexor anti-
extend to each digit where they are inserted on the pha- brachii lateralis superficialis arises by two heads. The su-
langeal elements. Through the association of the m. pal- perior head lies on the outer edge of the humerus, whereas
maris longus with the m. palmaris profundus, the m. pal- the lower originates from the lateral epicondyle. Fibers
maris longus flexes the digits. The mm. flexor antibrachii of the heads unite and pass into a tendón that runs over
medialis and ulnocarpalis lie deep to the foregoing mus- the radio-ulna-carpal articulation; distally, the tendón in-
cles on the median side of the forelimb. The former mus- serts on the carpus and on the tendón of the extensor of
cle arises by a tendón from the medial epicondyle of the the first digit. Contraction of this muscle flexes the elbow.
humerus and inserts on the radial side of the radio-ulna; and extends and supinates the hand. The m. flexor an-
it pulís the forearm in a medial direction. The m. ulno- tibrachii lateralis profundus arises deep to the superficial
carpalis lies deep to the m. palmaris longus where it arises antíbrachial muscle from the lateral epicondyle of the

A
-sacral diapophysis
-sesamoid bone

Figure 13-39. Anuran pelvic girdle structure.

A. Dorsal view of pelvic girdle of Rana esculenta
articulated with posterior part of vertebral
column. B. Lateral view of pelvic girdle of
R. esculenta. C. Ventral aspect of pelvic girdle of
Ascaphus truel showing pre- and postpubic
elements. D. Lateral view of pelvic girdle of
A. truel. Cartilaginous elements are shown in
stippled pattern. A—B redrawn from Gaupp
(1896), and C—D from Ritland (1955).
 Musculoskeletal System
-.iimerus. The muscle inserís along the length of the lower lum, and the nature of its articulation with the sacral dia- 355
ridge of the radio-ulna and acts to flex the elbow and pophysis. Proportionately longer ¡lia are associated with
supínate the hand. anurans that are more saltatorial, whereas shorter ilia are
In the hand, the m. palmaos profundus arises from the characteristic of terrestrial or fossorial species that tend to
•_Lnar border of the radio-ulna and extends obliquely to walk rather that jump.
r-sert on the palmar aponeurosis. Detailed descripüons The ilium articulates with the ventral surface of the
:i the balance of the palmar musculature associated with sacral diapophysis in one of three ways according to
—e prepollex and each of the four digits in various taxa S. Emerson (1979) (Fig. 13-40). In anurans having broadly
-¿•«re provided by Gaupp (1896), Andersen (1978), expanded sacral diapophyses with more or less straight
S. üem (1970), and T. C. Burlón (1983a). lateral margins, a superficial, transverse ligament unites
the anterolateral ends of the ilia across the body. This
Pelvic Girdle Structure. The pelvis of frogs consists configuration (Emerson's Type I) maximizes anterior-
::' three paired elements that unite in a medial symphysis; posterior movement of the pelvic girdle in a horizontal
r.ese are the ilium, ischium, and pubis (Fig. 13-39). The plañe and minimizes lateral and dorsal-ventral rotation.
rrmary elements are the ilium and ischium, because in In the Type II iliosacral articulation, each ilium is attached
most anurans the pubis is reduced. The ilium consists of to its adjacent sacral diapophysis by a ligament deep to
»r. anterior shaft that articulates with the sacral diapo- the dorsal back musculature, and a well-developed joint
physes and an expanded posterior end that forms the capsule is present. There are two kinds of Type II artic-
anterior half of the acetabulum. Variation in this element ulations. In anurans having moderately expanded sacral
r.volves its length, the presence and nature of crests along diapophyses with convex lateral margins, the ilium is at-
ríe shaft, the kinds of protuberances for muscle attach- tached to the diapophysis by a broad, transverse ligament
rnent that may be located anterodorsal to the acetabu- and articulates with its cartilaginous margin via a groove.

sacral sesamoid
ligament diapophysis

sesamoid ilium

HA

sacral
diapophysis

sesamoid

ligament

ilium

Figure 13-40. Diagrammatic representation of the three major types of iliosacral articulations in anurans.
Dorsal views of pelvic girdles and posterior vertebral columns with ligamentous attachments are illustrated
below schematic sections; levéis of sections are indicated by section lines in lower figures. A. Type I with
broad, transverse ligament. B. Type HA with broad, medially interrupted ligament. C. Type IIB with narrow,
distal ligament. Adapted from S. Emerson (1979).
MORPHOLOGY
356 According to S. Emerson, the Type IIA iliosacral articu- In contrast to salamanders in which digital reduction oc-
lation allows a certain amount of lateral rotatíon of the curs through the loss of the last (i.e., postaxial) toe, in
pelvis in the horizontal plañe, and is characteristic of the anurans it is the first preaxial digit that is lost (Alberch
majority of anurans. Anurans having a Type IIB iliosacral and Gale, 1985). Reduction in the length of individua.
articulation have round sacral diapophyses that are ori- digits can occur through the loss of one or more pha-
ented posterolaterally. The ilium is attached to the sacral langes. Intercalan/ structures are present between the pe-
diapophysis by a narrow, transverse ligament, but lacks nultimate and ultímate phalanges of the hylids, centro-
the groovelike articulation with the distal cartilage found lenids, pseudids, rhacophorids, hyperoliids, mantellina
in Type IIA. S. Emerson proposed that the Type IIB il- ranids, and phrynomerine microhylids.
iosacral articulation accommodated dorsoventral excur- As summarized by Nussbaum (1982), three hetero-
sión of the pelvis in a vertical plañe, and she associated topic skeletal elements are known to occur in associatior
it with anurans such as Rana that are accomplished, long- with tendons in the tarsal segment of anurans. The car-
distance leapers. tílago plantaris of Pipa, Rana esculenta, and some petro-
The ischium forms the posterior half of the acetabulum pedetíne ranids lies in the subartícular región of the foo*.
and vanes considerably in its shape, presumably in cor- A variety of anurans has a heterotopic element, the car-
relation with the muscles that origínate from this área of tílago sesamoides, in the ligamentum calcanei. The thirc
the girdle. The pubis usually is present as a carülaginous element is the os sesamoides tarsale which lies in the
element ventral to the acetabulum and located between proximal part of the aponeurosis plantaris in sooglossids.
the anteroventral margin of the ischium and the poster- species of Pipa, and some petropedetine ranids. Gener-
oventral margin of the ilium. In some anurans, the ele- ally these heterotopic elements occur at stress points ir.
ment calcifies so that its articulatíons with adjacent ele- tendons where the tendón transmits a forcé of a powerfa
ments are difficult to distinguish. muscle across a joint. According to Nussbaum, their pres-
Two ancillary structures are associated with the pelvic ence and calcification is presumed to strengthen a ten-
girdle in some frogs. These are pre- and postpubic ele- dón, help to maintain its shape, and increase the me-
ments (Fig. 13-39C, D). The leiopelmatids and the pipids chanical advantage of forcé translation.
Xenopus and Pseudhymenochirus possess a prepubic
element known as an epipubis. This small píate of car- Hindlimb Movcmcnt. Not all anurans are equally ac-
tilage is synchondrotically united with the pubis, and may complished at leaping. Some short-legged terrestrial forms
be calcified in adults. De Villiers (1934) suggested that (bufonids such as Osornop/iryne) tend to walk. Aquatic
the epipubis is homologous in these anuran genera and species such as Xenopus or Pipa pipa are agüe swimmers.
that it probably is a derivative of the linea alba. Further, and when on land, essentially utilize the splayed limbs to
he proposed that it might be a morphological or func- swim across the substrate. Nonetheless, all anurans are
tional homologue to the ypsiloid cartilage of salamanders. capable of some form of saltatorial locomotion, be it by
Postpubic, or Nobelian, bones occur only in Ascaphus a sequence of short hops or longer-ranging leaps, and
truei where they lie within the copulatory organ (or so- even anurans that primarily swim do so in a saltatoria^
called tail) and are attached to the posteroventral part of fashion (Calow and R. Alexander, 1973). As pointed out
the pelvic girdle. According to de Villiers (1934), these by Gans (1961), this pattern is unique to anurans among
postpubic elements are incorporated into the phallic or- lower tetrapods. It represents a fundamental departure
gan and possibly act as an os penis. from the generalized mode of progression by alternatinc
limb movement characteristic of salamanders and prim-
Hindlimb Structure. The anuran hindlimb is elon- itive tetrapods, because anuran saltation is powered by
gated relative to the forelimb. The proxímal thigh element simultaneous activatíon of both hindlimbs. Some of the
that articúlales with the pelvic girdle is the fémur (Fig. morphological modificatíons that accommodate this lo-
13-41). The shank (or crus) is represented by a com- comotory habit in anurans are familiar (e.g., the short
pound bone, the tibiofibula. The mesopodial or tarsal fusiform body and attenuate hindlimbs), but others in-
elements of anurans are modified significantly. The preaxial volving the musculature of the pelvic girdle and hindlimb
fibulare (= astragalus) and postaxial tibíale ( = calca- are less so.
neum) are elongate bones that are fused medially at their In a resting position, the several sets of long bones in
proximal and distal ends. Fusión of the fibulare and tibíale the anuran hindlimb are folded against one another. As
throughout their entire lengths to form a compound bone the animal leaps, the joints are extended more or less
occurs only in the centrolenids and pelodytids. The re- simultaneously, powered by muscles that lie on opposite
maining mesopodial elements consist of a prehallux (i.e., anterior and posterior) sides of each leg segment so
(preaxial), a céntrale, and one distal tarsal. Insofar as is that each bone can be shifted upon the one lying next
known, all except two species of anurans have five toes, closer to the body. The straightening of the legs transmits
and, thus, a series of five metatarsals and phalanges with a propulsive forcé through the solé of the foot to the
the typical formula of 2-2-3-4-3 (Digits I-V, respectively). substrate. It is this forcé that reaches its peak just before
Psyllophtyne didacfyla (brachycephalid) and Didynami- the foot leaves the ground and provides the power en-
pus sjoestedti (bufonid) have only four toes on the foot. abling anurans to leap forward.
 Musculoskeletal System
IV 357

prehallux

céntrale

tibíale

sesamoid c

Figure 13-41. Posterior extremity of

Rana escalenta, redrawn from Gaupp
(1896). A. Dorsum of right foot.
B. Venter of foot. C. Right tibiafibula
in ventral view and D. dorsal view.
E. Right fémur in lateral view and
F. medial view. Abbreviations: c =
cartilage; lat con = lateral condyle;
lig = ligament; med con = medial
condyle; tar(s) = tarsal(s).

Nusculature of Pelvic Girdle and Hindlimb. As cation of anurans. In this work, Noble provided a sum-
mentioned above, anurans demónstrate a wide variety mary of earlier literature. Aside from the general myo-
of locomotory habits such as walking, hopping, burrow- logical works cited previously in the description of the
ing, and climbing that can be viewed as specializations. forelimb musculature, the single most informative paper
These derived patterns of movement are associated with since Noble's, is that of Dunlap (1960) on the compar-
morphological modifications of the musculoskeletal sys- ative myology of the hindlimb in anurans. The nomen-
tem that involve the iliosacral articulation, the construc- clature used below follows Gaupp (1896) as modified by
tion of skeletal components, and the nature and arrange- Dunlap (1960). The descriptions are based primarily on
ment of associated muscles. This variation in pelvic and Rana catesbeiana and R. pipiens with some notes on the
hindlimb musculature (principally that of the thigh) has major variation in other anurans that have been studied.
attracted a great deal of attention since Noble's (1922) Details of this variation are provided by Dunlap (1960).
monograph on the phylogeny of the Salienüa in which The structure and orientatíon of the anuran hindlimb
he utilized characteristics of thigh muscles in his classifi- deviates markedly from the more generalized pattern ob-
MORPHOLOGY
358
ilium
-m iliac ext

m tens fas lat -m tens fas lat

m iliac ¡nt
m glut mag -m crur
m add long -m sart
rect abdom -m add ma:
coccyx

m pyr m pectin m ext crur

brev
-m semimemb m add mag-1
um iliofib m grac maj-1 m tib ant lor;
m perón m grac mm-1
m plant long— m tib ant brev
tibiafibula
m tib ant long
Achules' tendón
m tar ant
m tar post
mabdbrev dor dig V
fibulare
m fl brev sup

Figure 13-42. Left hindiimb musculature of Rana escalenta, redrawn from Gaupp (1896). A. Dorsal aspect.
B. Ventral aspect. Abbreviations: m abd brev dor dig V = m. abductor brevis dorsalis digiti V; m add
long = m. adductor longus; m add mag = m. adductor magnus; m crur = m. cruralis; m ext crur brev =
m. extensor cruris brevis; m fl brev sup = m. flexor brevis superficialis; m glut mag = m. glutaeus magnus;
m grac maj = m. gracilis major; m grac min = m. gracilis minor; m iliac ext = m. iliacus externus; m iliac
int = m. iliacus internus; m iliofib = m. iliofibularis; m pectin = m. pectineus; m perón = m. peroneus;
m plant long = m. plantaris longus; m pyr = m. pyriformis; m rect abdom = m. rectus abdominis; m
sart = m. satorius; m semimemb = m. semimembranosus; m tar ant = m. tarsalis anticus; m tar post =
m. tarsalis posticus; m tens fas lat = m. tensor fasciae latae; m tib ant brev = m. tibialis anticus brevis; m
tib ant long = m. tibialis anticus longus; m tib post = m. tibialis posticus.

served in salamanders in which extensors tend to be lo- numerous, they will be described relative to their size anc
cated on the dorsum of the limb and flexors on the ven- topographical position. Thus, long muscles originating or.
ter. While it surely would be a useful academic excercise the pelvic girdle are subdivided into three groups—(1
to organize the muscle descriptions by function, in the prefemoral muscles that occur on the anterior edge of
case of the ánuran hindiimb the structure is understood the thigh, (2) postfemoral muscles that are posterior anc
more easily with regional, topographic descriptions. The ventral, and (3) postfemoral muscles that are posterior
accounts describe the animal as though it were laid out and dorsal. A description of the short thigh muscles that
for dissection, that is, prone with the thigh at a right angle originate on the pelvic girdle follows the description of
to the midline of the body and the shank and foot ex- the long muscles. All of these muscles are innervated by
tended. All references to medial, lateral, anterior, etc. branches of the lumbosacralis plexus formed by S.Nn.
should be interpreted accordingly. 7-10.
Thigh musculature.—The well-developed thigh mus-
cles of anurans origínate on the pelvic girdle (Figs. Mm. tríceps femoris and tensor fasciae latae
13-42, 13-44) and are responsíble for moving the fémur The prefemoral thigh musculature is composed of the
in the hip joint in all directions, and in some cases, flexing mm. tríceps femoris and tensor fasciae latae. The m. trí-
the knee joint. Because these muscles are complex and ceps femoris forms the outer border of the thigh, ex-
 Musculoskeletal System
Kxüng onto both dorsal and ventral surfaces, and is a internus of salamanders, are considered togelher here. 359
compound muscle that is homologous with the m. il- The m. adduclor longus is a wide, thin muscle Ihal lies
joextensorius of salamanders. The m. cruralis constitutes venlral lo íhe m. cruralis and is partially covered venlrally
—e dorsal head of the m. tríceps femoris. It arises from by íhe m. sartorius. Il arises via a tendón from íhe an-
—•e ventral margin of the acetabulum and extends along lerovenlral part of íhe preacelabular rim belween íhe
—e anterior margin of the thigh; the fibers converge on mm. sartorius and íhe pectineus. The m. adduclor longus
2 tendón at the knee. The tendón extends over the knee bears a fleshy insertion on íhe lateral face of íhe dislal
2T.c bifurcates. One branch inserís at the base of the part of íhe m. adduclor magnus (see description below),
epiphysis on the tibial side of the tibiofibula, and the and somelimes bears a lendinous insertion on íhe knee
rc-.er. smaller tendón inserís inside the belly of íhe aponeurosis. The m. peclineus has a fleshy origin from
— planfaris longus (see descripíion below). The posterior the venlrolateral ilium and anterior part of íhe pubis. This
r.ead of íhe íhe m. tríceps is íhe m. glulaeus magnus. short, fan-shaped muscle has a fleshy insertion on íhe
This muscle arises anlerodorsal lo íhe acelabulum along proximal half of íhe venlral surface of íhe fémur. Il is
—e dorsolaleral surface of íhe ilium and exlends along bordered anteriorly by íhe m. cruralis and posteriorly by
~.e dorsal surface of íhe Ihigh lo unile in a common íhe m. obluralor exlernus, and lies deep lo íhe m. sar-
sndon wilh íhe m. cruralis. The m. tensor fasciae latae torius. The m. adduclor longus is absenl in some frogs
arises along íhe venlral margin of íhe posterior parí of (e.g., Ascaphus, Leiopelma, Afytes, Bambino, and some
~e ilial shafl and exlends poslerolalerally lo inserí on íhe pipids, pelobalids, and bufonids); ils absence may have
rascia covering íhe m. cruralis on íhe anterodorsal aspecl resulled from loss or lack of differentialion from íhe
of the Ihigh. Together, Ihis complex of muscles exlends m. pectineus. The latler is assumed to be the case in
ríe knee joinl and flexes íhe hip joint primitive frogs.

Mm. sartorius and semitendinosus M. adductor magnus

The mm. sartorius and semitendinosus (= m. sarto- The m. adductor magnus is a large muscle Ihal exlends
riosemilendinosus of some aulhors) form a compound along íhe superficial and proximal ventromedial surface
muscle Ihat abducts íhe fémur and pulís il venlrally and of fhe Ihigh, and is covered by íhe mm. sartorius and
flexes íhe knee. These are lwo of a group of seven mus- gracilis major distally. The primary aclion of Ihis muscle
cles Ihal constilules íhe poslfemoral, venlral Ihigh mus- is lo adducl the hip joinl. The m. adduclor magnus arises
culalure. The m. sartorius is a wide, Ihin muscle Ihal by lwo heads which are separaled from each olher by
arises from the anterovenlral margin of the preacelabular íhe venlral tendón of íhe m. semilendinosus. The venlral
zone of íhe pelvis (ilium) and exlends across íhe venlral head, which arises via a tendón from íhe venlral border
surface of the thigh. The fibers converge on a tendón al of the pubic part of íhe pelvic rim, is considered a hom-
íhe knee; the tendón inserís on íhe aponeurosis of íhe ologue of íhe m. pubotibialis of salamanders. The dorsal
m. cruralis and íhe tendón of íhe m. semitendinosus and head has a fleshy origin from íhe ischialic border of íhe
the insertíon of íhe m. gracilis major. pelvic rim benealh the origin of íhe m. gracilis major, and
The second member of Ihis complex, íhe m. semiten- is the homologue of íhe m. puboischiofemoralis of sala-
dinosus, has a double, lendinous origin from (1) íhe pos- manders. The dorsal and venlral heads unile lo form a
lerovenlral pelvic rim near íhe unión of íhe ischium and single muscle Ihal inserís one-fourth lo Ihree-quarters down
pubis, and (2) íhe poslerodorsal pelvic rim. The muscle íhe lenglh of íhe fémur on ils medial side. Variation in-
exlends along íhe ventromedial surface of íhe Ihigh and volves íhe level of insertion of Ihis muscle and íhe pres-
inserís on íhe venlral surface of íhe tibiofibula. In more ence or absence of lwo heads. In those anurans in which
primilive frogs (e.g., leiopelmatíds, most discoglossids, íhe m. semitendinosus has a superficial origin (primarily
pipids, and pelobalids), íhe mm. sartorius and semiten- primitive anurans), an accessory head is absenl; il is presenl
dinosus are united into a common muscle with lwo heads in mosl advanced anurans in which íhe semitendinosus
Ihal unile about half way down the thigh; bolh muscles has a deep origin.
inserí on íhe ventral surface of íhe tibiofibula. In most
bufonids, the muscles are sepárate; however, the m. sar- Mm. gracilis major and minor
torius may inserí on íhe tendón of the m. semilendinosus. The mm. gracilis major and minor form a muscle com-
The mm. sartorius and semilendinosus are considered lo plex Ihal flexes íhe knee joinl and exlends íhe hip joinl
be homologues of íhe m. puboischiotibialis of salaman- by pulling íhe upper limb backwards; bolh muscles are
ders. considered lo be homologous wilh íhe m. ischioflexoris
of salamanders. The gracilis major is a broad, flal muscle
Mm. pectineus and adductor longus on íhe mediovenlral surface of íhe Ihigh. U bears a len-
The mm. pectineus and adduclor longus compose a dinous inscription al its midlenglh and is bordered dor-
compound muscle Ihat adducts íhe fémur. The m. pec- sally by the m. semimembranosus (see description be-
tineus is a short muscle of íhe Ihigh, from which the low), lalerally by íhe m. semilendinosus, and venrrolaterally
m. adducfor longus is Ihoughl to have differentiated. Both by íhe m. adduclor magnus. The m. gracilis major bears
muscles are homologues of the m. puboischiofemoralis a lendinous origin from íhe posterior border of íhe pelvic
MORPHOLOGY
360 rim of the ischium. It inserís by means of two tendons; iliacus externus to a broad, fleshy insertion along the
one broad tendón inserts on the knee aponeurosis and proximal two-thirds of the fémur on its dorsomedial sur-
medial side of the head of the tibiofibula, and the other face. Contraction of the m. iliacus internus abducts the
tendón attaches to the posterior surface of the tibiofibula fémur.
just distal to the head. Variation in this muscle involves
its origin (fleshy versus tendinous) and the position of its M. iliacas externus
insertion with respect to that of the m. semitendinosus. The m. iliacus externus is also thought to be homol-
The m. gracilis minor is a thin, narrow muscle that lies ogous with the m. puboischiofemoralis of salamanders.
beneath the skin along the medial surface of the thigh From its broad, fleshy origin on the lateral surface of the
and bears a tendinous inscriptíon. It bears a tendinous posterior half of the ilial shaft, this muscle extends ven-
origin from the ischiatic región of the pelvic rim just ven- trolaterally to inserí on the dorsal surface of the head of
tral to the cloaca. The muscle unites with the gracilis the fémur by a íendon, and acís to flex the hip joint,
major distally prior to the formatíon of a common tendón. drawing the fémur forward. There is considerable varia-
Variation in this muscle involves its origin which may be tion in the m. iliacus externus. lí is absení or undiffer-
primarily from the pelvis, chiefly from the skin, or via two enüaled from íhe m. iliacus iníernus in Leiopelma. In fhe
heads—one from the pelvis and the second from the other anurans thaí possess this muscle, ¡t may origínate
skin. by either one or two heads, and its origin vanes from the
posterior half to the entire length of the ilial shaft.
Mm. iliofibularis and semimembranosus
Two muscles compose the postfemoral dorsal thigh M. iliofemoralis
musculature— mm. iliofibularis and semimembranosus. The m. iliofemoralis is homologous with the muscle of
The m. iliofibularis is a long, slender, subcylindrical mus- the same ñame in salamanders. The muscle originates in
cle that lies on the dorsal surface of the thigh between part from the ilium ventral to the origin of the
the mm. glutaeus magnus and semimembranosus, and m. iliofibularis and in part from the tendón of origin of
is homologous with the muscle of the same ñame in the m. iliofibularis. The fibers of the m. iliofemoralis par-
salamanders. The muscle has a tendinous origin from the allel those of the m. iliacus internus to their fleshy inser-
dorsolateral surface of the base of the ilial crest just pos- tion along the proximal third of the dorsomedial border
terior to the origin of the m. glutaeus magnus. Its tendi- of the fémur. Contraction of this muscle draws the fémur
nous insertion on the knee aponeurosis is covered by the dorsally.
aponeurosis of the m. tríceps femoralis and the origin of
the m. plantaris longus. Contraction of the m. iliofibularis M. pyriformis
flexes the knee joint and abducts the fémur. The m. pyriformis is a long, slender, subcylindrical
The m. semimembranosus is a large muscle that covers muscle that has a fleshy origin from the dorsolateral bor-
the dorsomedial surface of the thigh and bears a tendi- der of the distal end of the coccyx. The muscle extends
nous inscription near its midlength. The muscle originales distally, ventral and between the mm. glutaeus magnus
from the posterior surface of the ischium, along the pelvic and iliofibularis on one side and the m. semimembra-
rim and below the cloaca. It inserts via a tendón on the nosus on the other, and has a fleshy insertion on the
ventral surface of the fémur and the adjacent surface of dorsal surface of the fémur, which it abducts. The
the head of the tibiofibula and acts to flex the knee joint m. pyriformis is absent in Pipa and Xenopus, and varíes
and adduct the fémur. Variation includes origin by two in the posiüon of its insertion along the fémur in other
heads rather than one, and a tendinous instead of a fleshy anurans. It is considered to be a homologue to the
origin. Like the mm. gracilis major and minor, the m. caudalifemoralis of salamanders.
m. semimembranosus is thought to be a homologue of The m. obturator internus is one of four additional.
the m. ischioflexoris of salamanders. deeper muscles of the thigh. It extends ventrolaterally
over the hip joint from its fleshy origin that covers the
M. iliacas internas entire lateral surface of the pelvic rim. The muscle inserts
The m. iliacus internus is one of eight short muscles via a tendón on the dorsomedial surface of the fémur
(exclusive of the m. pectineus described above) involved head, and ventral fibers extend posterodorsally to inserí
in the thigh musculature, among the most superficial of on the heavy tendón to the head of the fémur. The mus-
which are the mm. iliacus internus, iliacus externus, ili- cle is considered to be a homologue of the m. ischio-
ofemoralis, and pyriformis. The m. iliacus internus is ho- femoralis of salamanders. On contraction, it pulís the fé-
mologous with the m. puboischiofemoralis of salaman- mur dorsally and rotates it.
ders. This broad, fíat muscle passes under the ventral
border of the pelvis anterior to the origin of the m. cruralis Mm. obturator externus, quadratus femoris,
from its fleshy origin along the margin of the ilium in the and gemellus
angle formed between the ilial shaft and the preaceta- The remaining three deep, short muscles—the mm
bulum. It extends dorsally between the mm. cruralis and obturator externus, quadratus femoris, and gemellus—
 Musculoskeletal System
m crur 361
m add long

lig med m pectín

m add mag (cap
vent)
m sart m add mag (cap
,dor)
m semimemb
TI grac maj
semitend (cap dor)- Lm semitend (cap vent)
•n grac min m plant long
m tib post

-m iliac int
-m iliofem
-m pyr

m gem

m add mag (capdor)

m semitend (cap vent) m add mag (cap vent)
-m add mag (cap acc)

¡lium
Figure 13-43. Thigh musculature of right limb
of Rana escalenta, redrawn from Gaupp (1896).
A. Ventral aspect with some superficial muscles
m coccüiac removed. B. Dorsal aspect with superficial
muscles removed. C. Dorsal view showing deep
muscles of thigh. Abbreviations: cap acc =
caput accessorium; cap dor = caput dorsalis;
-m crur cap vent = caput ventralis; lat lig = lateral
m pyr -m iüofíb ligament; med lig = medial ligament; m add
-m iliofem long = m. adductor longus; m add mag =
m. adductor magnus; m cocciliac =
m obt int -m iliac int m. coccygeoiliacus; m crur = m. cruralis; m
m gem gem = m. gemellus; m grac maj = m. gracilis
m quad fem major; m grac min = m. gracilis minor; m iliac
m add mag ext = m. iliacus externus; m iliac int =
m. iliacus internus; m iliofem = m. iliofemoralis;
m add mag (cap acc) m iliofib = m. iliofibularis; m obt ext =
m. obturator externus; m obt int = m. obturator
m semitend (cap vent) internus; m pectin = m. pectineus; m plant
long = m. plantaris longus; m pyr = m.
m iliofib- -lat lig pyriformis; m quad fem = m. quadratus femoris;
m sart = m. sartorius; m semimemb =
m. semimembranosus; m. semitend =
m plant long- m. semitendinosus; m tib post = m. tibialis
posticus.

form a single muscle complex that pulís the fémur ven- chium is separated from that of the m. obturator externus
trally. The m. obturator externus (a homologue of the by the ventral head of the m. semitendinosus. The
m. pubifemoralis of saiamanders) is a short, triangular m. quadratus has a fleshy insertion on the ventromedial
muscle that has a fleshy origin from the lateral surface of surface of the fémur near the head of this bone.
the pelvic rim in the área posteroventral to the aceta- The last deep, short muscle is the m. gemellus, a hom-
bulum near the pubis. The fleshy inserüon of the muscle ologue of the m. ischiofemoralis of saiamanders. This
lies on the ventral surface of the proximal half of the slender muscle has a fleshy origin from the dorsal margin
fémur. of the ischium dorsal to the origin of the m. quadratus
The m. quadratus femoris is a short, triangular muscle femoris. Its fleshy insertion lies on the medial surface of
homologous with the m. pubifemoralis of saiamanders. the fémur at the base of the head. This complex muscle
Its fleshy origin from the ventrolateral border of the is- is variable in the degree of separation and fusión of the
MORPHOLOGY
362

femur-
m obt int-

Figure 13-44. Muscles associated with the

pelvic girdle of Rana escalenta, redrawn from rm obl ext
Gaupp (1896). A. Lateral view of pelvic girdle r-m transv
and head of fémur. B. Diagram showing ^m iliac ext
positions of muscle origins from pelvic girdle.
mm iliofib & iliofem- m semimemb
Abbreviations: m add long — m. adductor r m gem
longus; m add mag (cap dor) = m. adductor m glut
magnus (caput dorsalis); m add mag (cap m semitend
vent) = m. adductor magnus (caput ventralis); m si
crur = m. cruralis; m gem = m. gemellus; m m add mag
glut mag = m. glutaeus magnus; m grac maj = (cap dor)
m. gracilis rnajor: m iliac ext = m. iliacus
externus; m iliac int = m. iliacus internus; m rn transv m grac maj
iliofem = m. iliofemoralis; m iliofib = m. m tens fas lat—
iliofibularis; m obl ext = m. obliquus externus;
m obt ext = m. obturator externus; m obt int = m quad fem
m. obturator internus; m pectin = m. pectineus;
m quad fem = m. quadratus femoris; m sart = m add long- m semitend
m. sartorius; m semimemb = m. m sart- -m add mag (cap
semimembranosus; m semitend = m. m pect-
semitendinosus; m tens fas lat = m. tensor m obt ext vent)
fasciae latae; m transv = m. transversus. m crur- m obt ¡nt

three muscles that compose it. For example, the mm. a long, slender tendón that extends from the distal part
obturator externus and quadratus femoris are fused in of the tibiofibula. Contractíon of the mm. plantaris longus
Ascaphus, and the mm. gemellus and quadratus femoris and tibialis posticus results in straightening the ankle joint.
are partly united in Bufo. There is also considerable var-
iation in the insertion of the complex. M. peroneas
Lower hindümb musculature.—The shank (tibiofi- The m. peroneus is one of four muscles on the lateral
bula) bears eight muscles. of which are associated with side of the tibiofibula. It is a long, thick muscle that origi-
the medial, or flexor, side of this element. Tríese are the nates from a short, heavy ligament on the external sur-
mm. plantaris longus and übialis posticus (Figs. 13-43, face of the knee joint via a long tendón that extends deep
13-45). to, and penetrales, the aponeurosis. The muscle has a
tendinous insertion on the dorsal surface of the distal end
Mm. plantaris longus and tibialis posticus of the tibiofibula, and acts to extend the knee joint.
The m. plantaris longus (= m. gastrocnemius of some
authors) is a large, thick-bellied muscle that extends the M. tibialis anticus longus
foot. It is one of two muscles which are associated with The m. tibialis anticus longus is a second, lateral muscle
the medial, or flexor, side of this element; the other is of the tibiofibula. It is a large, tapering muscle located on
the m. tibialis posticus. The m. plantaris longus originates the lateral surface of the shank that arises via a tendón
by two tendinous heads—one a long, slender dorsal ten- that passes over the knee from the ventral surface of the
dón from the distal border of the aponeurosis covering medial condyle of the fémur. Approximately two-thirds
the knee, and the second, a short, cylindrical tendón the distance down the shank, the m. tibialis anticus lon-
formed by the unión of two branches of the heavy, ten- gus divides into two bellies, the heads of which inserí
dinous are along the medial surface of the knee joint. (1) laterally, on the dorsolateral surface of the proximal
The m. plantaris longus inserts distally by a thick, fíat end of the fibulare, and (2) medially, on the medial bor-
tendón that spreads out on the plantar surface of the foot der of the proximal end of the tibíale. Contractíon of this
to form the aponeurosis plantaris, from which numerous muscle extends the ankle joint.
tarsal and foot muscles originate. The m. tibialis posticus
¡s covered for the most part by the m. plantaris longus. M. extensor crurís brevis
This muscle has a fleshy origin along the medial surface A third lateral tibiofibula muscle, the m. extensor cruris
of the shaft of the tibiofibula and inserts on the tibíale via brevis is slender and lies deep to the m. tibialis anticus
 Musculoskeletal System
363
-m abd brev dor dig V
i-m tib ant long
r m perón
fémur—i

Figure 13-45. Distal musculature of

m ext crur brev right hindlimb of Rana escalenta,
Lm tib ant brev redrawn from Gaupp (1896).
prehallux-1 Lm tar ant
A. Dorsomedial aspect.
B. Ventrolateral aspect.
mm grac min &grac maj- Abbreviations: apon plant =
aponeurosis plantaris; lat lig =
m semitend- lateral ligament; m abd brev dor dig
V = m. abductor brevis dorsalis
digiti V; m ext crur brev = m.
prehallux- rm tar post extensor cruris brevis; m fl brev
m plant prof sup = m flexor brevis superficialis;
m iliofib = m. iliofibularis; m
perón = m. peroneus; m plant long
= m. plantaris longus; m plant prof
= m. plantaris profundus; m
semimemb = m. semimembranosus;
m. semitend = m. semitendinosus; m
tar ant = m. tarsalis anticus; m tar
post = m. tarsalis posticus; m tib ant
brev = m. tibíalas anticus brevis; m
Achules' tendón tib ant long = m. tibialis anticus
m plant long- longus; m tib post = m. tibialis
posticus; mm grac min & grac maj
m iliofíb-1 = mm. gracilis minor et gracilis
m semimemb- major.

longus along the ventrolateral margin of the übiofibula. lensors. The m. adduclor brevis dorsalis digiti V is a rel-
The muscle originates from a long, slender tendón that alively large, fleshy muscle Ihat lies along the dorsolaleral
passes over the external surface of the knee from the surface of Ihe larsus. Il originales along the entire lenglh
ventral surface of the medial condyle of the fémur. It of Ihe fibulare and has a fleshy insertion on Metatar-
bears a fleshy insertion along the proximal one-half to salV.
two-thirds of the ventrolateral surface of the übiofibula
and on contraction extends the knee joint. Ventral tarsal muscles
Six or seven muscles are associated wilh Ihe venlral,
M. tibialis anticus brevis or planlar, surface of Ihe larsus. Superficially, Ihe lendi-
The final muscle of the shank is the m. tibialis anticus nosus aponeurosis planlaris is a continualion of Ihe dislal
brevis which pulís the foot dorsally and supínales it. This tendón of Ihe m. plantaris longus of Ihe shank. Tendons
long, slender muscle is covered partially by the m. tibialis arise from Ihe dislal border of the aponeurosis and ex-
anticus longus, but is visible along the medial margin of lend lo Ihe prehallux and each digil where each tendón
the latter. The m. tibialis anticus brevis has a fleshy origin is connected lo the phalangeal elemente. The m. larsalis
from the dorsolateral surface of the middle third of the posticus is a large, fleshy muscle Ihal exlends Ihe larsus.
tibiofibula and inserts by a short tendón on the proxí- U shares its origin with, and lies dorsal lo, Ihe m. planlaris
momedial surface of the tibíale. profundus. The m. larsalis posticus inserís along Ihe dislal
Ihree-quarters of the venlral surface of Ihe tibíale. The
Dorsal tarsal máseles m. planlaris profundus arises from Ihe medial half of Ihe
The anuran tarsus bears three muscles dorsally. The ligamenlum calcanei and has a fleshy insertion Ihal ex-
m. tarsalis anticus arises by a tendón from the lateral lends along Ihe dislal two-lhirds lo Ihree-quarters of Ihe
aspect of the distal end of the tibiofibula and has a fleshy tarsus lo base of fhe prehallux. The m. flexor digilorum
insertion along the distal half of the dorsal surface of the brevis superficialis arises from the lateral half of Ihe lig-
tibíale. Contraction of thís muscle flexes the anide joint amenlum calcanei, and inserte by a tendón on Ihe apo-
and supínales the foot. The m. exlensor longus digiti IV neurosis planlaris. The mm. Iransversus planlae proxi-
is a long, narrow muscle that lies on the dorsal surface malis and dislalis are distal transverse muscles of Ihe larsus
of the foot between the m. tarsalis anticus, wilh which il thal are nol always dislincl from one anolher. The
shares a common origin, and Ihe m. adduclor brevis dor- m. intertarsalis lies belween the tibíale and fibulare. Il has
salis digili V. Il has lendinous insertions on Ihe dislal ex- a fleshy origin along Ihe lateral margin of Ihe proximal
MORPHOLOGY
364 two thirds of the tibíale and the medial margin of the obtain food. The majority are only able to roll the tongue
fibulare, and a tendinous insértion on the céntrale. forward over the margin of the lower jaw to contact the
For details of the foot musculature, the reader ¡s re- prey. Once in the buccal cavity, food ¡s held and ma-
ferred to Dunlap (1960) and Andersen (1978) as well as nipulated by the teeth and tongue. Such a system does
the several myological descriptions of particular groups not require specializations of mandibular and jaw mus-
of anurans cited above. The dorsal musculature is com- culature or possession of robust, specialized teeth—fea-
posed primarily of the mm. extensores breves medii and tures that salamanders generally lack. However, it does
profundi. The former is a group of thin muscles that origí- involve sensory perception. Thus, salamanders are char-
nate from near the middle of the distal fused extremities acterized by well-developed eyes and nasal organs. In
of the tibíale and fibulare. The muscle mass extends dis- the absence of significant vocal abilities, their ears are
tomedially and subdivides into two or more muscular rather poorly developed in contrast to those of frogs.
slips per digit. The mm. extensores breves profundi con- Owing to the lack of specialization of the postcranial
sists of a series of 10 muscles, one of which lies on the musculoskeletal system of most salamanders, they are
lateral and one on the medial border of each digit. These limited to somewhat primitive modes of locomotion. The
muscles origínate from the metatarsal and insert on the axial skeleton is relatively undifferentiated, the trunk
base of the terminal phalanx. Significan! features of the musculature well developed, and the girdles neither well
plantar musculature include the tendines superficiales that developed ñor especially firmly attached to the vertebral
arise from the aponeurosis plantaris and the mm. lum- column. This allows most salamanders, if startled, to move
bricales, a group of small muscles that flex the digits. quickly across the substrate by undulating their bodies:
Distally, there are additional flexors, as well as muscles thus, the limbs are not used, and the organism is pro-
that connect adjacent metatarsal elements and adjacent, pelled forward by a series of successive undulations on
basal phalangeal bones. opposite sides of the long body and tail. Under other
circumstances, salamanders are able to move by a delib-
érate, diagonal pattern of limb movement whereby each
INTEGRATION OF FUNCTIONAL UNITS limb moves alternately, and the trunk and body are thrown
As mentioned in the introductory remarks to this chapter, into a curve to advance the stride of the forelimb.
the overall morphology of a species, or its Bauplan, rep- Most deviations from the general pattern occur in aquatic
resents the observable interface of the organism with its salamanders. These animáis that are supported by their
environment. In this respect, the Bauplans of the three aquatic environment may attain much larger sizes than
living orders of amphibians are remarkably different from their terrestrial counterparts. In some cases the limbs are
one another—a fact that suggests that each group has lost. Such salamanders depend on undulatory move-
had a long evolutionary history. The following para- ments to propel themselves through the water, but those
graphs attempt to summarize how the various functional with limbs are capable of crawling on the bottom.
units described in the preceding text are combined to
produce the architectural plan characteristic of each of Caecilians
the orders of amphibians. Of the three orders, caecilians probably are the most
narrowly specialized. Although some are aquatic, most
Salatnanders are adapted for a burrowing, subterranean existence. They
In contrast to caecilians and anurans, most salamanders also are the most limited distributionally and have fewer
are characterized by a lack of specialization marked by representatives than either salamanders or anurans. The
possession of relatively small heads, attenuate bodies, extemal morphotype of caecilians is remarkably uniform
four limbs, a tail, and a sprawling gait. The skulls of most and wormlike in appearance. The head is compact and
terrestrial salamanders are rather arched and narrow, and well ossified. Many centers of ossification have fused to
not especially well roofed despite the fact that they are provide a robust, spatulate cranium which the organisms
composed of more sepárate elements than the crania of use to push through the soil. The compact nature of the
either caecilians or anurans. However, in contrast to these skull necessarily limits the size and development of jaw
groups, salamander skulls bear an additional set of artic- musculature; thus, in caecilians the lower jaw bears a
ulations with the vertebral column. Possibly, this modi- retroarticular process to which the main adductor of the
fication of the primitive tetrapod condition may relate the jaw attaches external to the cranium. The hyomandibular
need to stabilize the head on the axial skeleton in terres- apparatus is modified only slightly from the larval con-
trial situations in the absence of specialized trunk mus- dition because the tongue in caecilians is rudimentary
culature that accomplishes this task in the other orders and cannot be protruded from the oral cavity. The eyes
of amphibians. The modification also might reflect the of caecilians are reduced, but their chemosensory per-
independent evolution of a craniovertebral joint in this ception is enhanced by the development of a tentacle in
group. addition to their well-developed nasal organ. Hearing
The hyoid apparatus of salamanders allows them to probably is less acute in caecilians than in salamanders
protrude their fleshy tongues from the buccal cavity to and and anurans. The operculum, if present, is incor-
 Musculoskeletal System
porated into the columella, a compact bone that articu- presacral vertebrae, and proximal part of the hindlimb 365
les with the auditory capsule and quadrate. by muscles and ligaments so that when the animal leaps,
The axial musculoskeletal system is highly modified for the girdle lies in the same plañe as the axial column, but
5_bterranean locomotíon and feeding. The axial muscles when it sits at rest, the posterior end of the girdle is de-
2re firmly attached to the overlying skin, and together flected ventrally.
—ese elementa form a tough sheath that surrounds the Despite the specialization of this morphological system
snenuate body and extends onto the posterior part of for jumping, many anurans have evolved adaptations that
—.e skull. Because the vertebral column is extremely flex- facilítate burrowing or arboreal habits. This primarily in-
.b!e within this myointegumental sheath, caecilians are volves changes in the relaüve proportions of the limbs
rapable of propelling themselves forward through the soil and the iliosacral articulation. One group in particular,
ry a process known as concertina locomotion. As ex- the pipids, are aquatic specialists. In Pipa the entire body
piained by Gans (1974, and references therein), part of is depressed, and the axial skeleton constructed in such
—e body is folded so that it is in static, frictional contact a way that little or no flexibility is possible. Thus, the
:th the substrate; adjacent parts of the body are pushed animáis utilize their strong hindlimbs to thrust their fíat,
-r pulled forward at the same time. This results in an fusiform bodies through water.
itemation of folding and extending that travels the length The vast majority of anurans have well-developed
DÍ the body. tongues which they are able to catapult from their mouths
Although caecilians are known to feed on the surface, in order to pick up prey. This complicated mechanism
presumably most usually feed in subterranean burrows involves a complex system of mandibular and hyoid
n which there may not be much latitude for movement. muscles that are associated with a specialized hyoid ap-
They seem to utilize their powerful jaw musculature and paratus. Given the locomotory and feeding habits of anu-
anterior trunk musculature to seize and immobilize prey rans, there obviously is a premium on visual acumen;
•Aith sharp, recurved teeth. If the prey cannot be ingested thus, it is not surprising that, in general, these animáis
•¿•hole, they shear it against the walls of the burrow by have large, well-developed eyes. Most anurans vocalize
rotations of the body (Bemis et al., 1983). as part of their mating and territorial behavior; thus, their
ears are more highly developed than those of salaman-
Anurans ders, and most have an externa! tympanum—a feature
The locomotory, feeding, and reproductive specializa- unknown in either salamanders or caecilians.
tions of anurans have enabled them to exploit a broader It is often pointed out that anurans are the most spe-
range of habitats than either salamanders or caecilians. cialized of the amphibians. Obviously, they are derived
They are more widespread, diverse, and numerous than relative to salamanders, but the comparison is less clear-
either of those groups. The basic body plan of anurans cut with respect to caecilians owing to the nature of the
is characterized by a broad, fíat head that is nearly as specializations of each order. In general, caecilians are
wide as the body. The trunk is short and largely inflexible adapted to a subterranean mode of Ufe. Although some
except in the área of the sacrum; thus, the head and are aquatic, the order as a whole now seems to be re-
trunk form a fusiform structure that is propelled forward stricted in its evolutionary options. The specialzations that
in a trajectory by the long, powerful hindlimbs. Because resulted in the anuran morphotype, in contrast, seem to
of their saltatorial habits, anurans have more elabórate have opened up a plethora of adaptive avenues that anu-
pectoral and pelvic girdles than salamanders. The pec- rans have pursued. The current success of this order is
toral girdle bears an elastic, muscular suspensión to both reflected in some measure by their greater numbers rel-
the skull and the vertebral column, and is designed to ative to salamanders and caecilians. Taken together,
absorb the shock of the anuran's landing on its forelimbs. however, the evolutionary diversity of modern amphib-
Unlike the pelvic girdles of salamanders, those of anurans ians must be regarded as nothing short of of spectacular,
lie in a horizontal plañe flanking the coccyx, the bony given the physiological constraints that tie them to their
rod that represents the posterior end of the vertebral col- environment in contrast to the relative independence
umn. The pelvic girdle is attached to the coccyx, sacrum, achieved by amniotes.
 CHAPTER 14
-An animal is a highly integrated machine
and, because it is, it is convenient rather
¡han analytical to regard it in pieces, as a
collection of sepárate characters and
adaptations.
Iiitegumeiitarv,
Thomas H. Frazzetta (1975)

Seii&ory, and
Visceral
Systems

A Ls was demonstrated in Chapter 13, the gestalt of

an organism is determined by its musculoskeletal or-
Only one visceral syslem is nol involved in Ihe main-
tenance of the internal environmenl; Ihis is Ihe repro-
ganization, which dictates how the animal can feed and ductive system. Anatomically il is associaled inlimalely
move and, to a certain extent, determines its utilization wilh Ihe excretory system; henee, Ihe two usually are
of the physical environment. The musculoskeletal sys- discussed as the urogenital system. The reproductivo sys-
tem, together with the integument, also protects and sup- lem acls in response lo Ihe internal environmenl and cues
ports the soft anatomical components of the sensory, from Ihe exlernal environmenl, bul ils function obviously
nervous, circulatory, respiratory, digestive, urogenital, and is lo ensure Ihe transmission of the parenlal genotype lo
endocrine systems. The nervous system coordínales the a succeeding generation.
activities of all other systems. Sensory structures are the
receptors of environmental stimuli. Perceived sensory cues
are transmitted to the central nervous system and thence INTEGUMENT
to the peripheral and/or visceral nervous systems. Signáis Allhough Ihe inlegumenl is Ihe structural and functional
transmitted via the peripheral nervous system affect the inlerface between Ihe organism and ils environmenl, Ihe
musculoskeletal system directly, whereas those transmit- morphological and functional complexity of amphibian
ted via the sympathetic (= efferent) and parasympatheüc skin is incompletely understood (see Lindemann and
(= autonomic) porüons of the visceral nervous system Voüle, 1976, and Whitear, 1977, for reviews). The skin
affect visceral organs of the circulatory, digesüve, uro- of amphibians generally is described as being naked, Ihal
genital, exocrine, and endocrine systems. is, lacking Ihe covering of scales, fealhers, or hair char-
The respiratory, digestive, excretory, exocrine, endo- acleristic of mosl olher classes of vertebrales. Further-
crine, and circulatory visceral systems are involved with more, amphibian skin is permeable to water and as such
the maintenance of the internal environment. Thus, met- is importanl in respiration, osmoregulation, and lo a linn-
abolic requisites are introduced via the respiratory, integ- ited degree, Ihermoregulation; these functional aspects
umentary, and digestive systems, and metabolic producís are trealed in Chapler 8. Also, the general appearance
are disposed of by the excretory, respiratory, and inte- of amphibians is the result of int^gumenlary slructures;
gumentary systems. Melabolic and endocrine producís color and pattern are determined by Ihe chromalop-
are Iransported Ihroughoul Ihe body by me circulatory hores, and lexlure is Ihe resull of inlegumenlary modi-
system to mainlain a slable internal environment. fications.
367
368 Structurc splitting of the dorsal skin progresses posteriorly. Most
As in all vertebrales, the integument consists of an outer amphibians use their limbs to loosen and remove the
layer, the epidermis of ectodermal origin, and an under- slough either in patches or in one large piece; usually the
lying layer, the dermis. Most of the latter is of mesodermal slough is eaten. During the sloughing cycle, the intercel-
origin, but the pigment cells are derived from the neural lular subcorneal space between the stratum corneum and
crest and thus are ectodermal; also, the glands imbedded the underlying stratum germinativum is filled with mucus
in the dermis are derived from the ectoderm. thought to be secreted by the mitochondria-rich cells.
The outermost layer of the epidermis, the stratum cor- During actual sloughing, the desmosomal connections
neum, consists of a single layer of flattened cells. The between the cells of the stratum corneum and the un-
stratum corneum is keratinized in most adult amphibians, derlying replacement layer, derived from the stratum ger-
but it is not keratinized in oblígate neotenic salamanders, minativum, are broken, and the desmosome fragments
such as Necturus. The keratinized stratum corneum is adhere to the sloughed stratum corneum. According to
separated from the underlying stratum germinativum by Budtz (1977), sloughing in Bufo is arrested by hypophy-
irregular intercellular spaces that are interrupted by in- sectomy; adrenocorticotrophic hormone (ACTH) and
terconnecting filaments (desmosomes). The fibers of these corticosteroids are the only hormones that elicit sloughing
keratinized cells form a double horizontal network rein- in hypophysectomized toads, but neither hormone has
forced by vertical bundles of filaments (tonofilaments) an effect on sloughing in normal toads. The formation of
(Le Quang Trong and Bouligand, 1976) (Fig. 14-1). Un- cocoons by aestivating amphibians is the result of múl-
derlying the stratum corneum is the stratum germina- tiple sloughs (see Chapter 8).
tivum which normally is 4—8 cells thick; the innermost The dermis also consists of two layers. The outer stra-
cells are columnar and the outer ones are progressively tum spongiosum is made up of areolar connective tissue
shorter. Lying within the stratum germinativum are spe- with interlacing fibers and various types of cells, including
cialized mitochondria-rich cells and flask cells of unknown the pigment-bearing chromatophores. The underlying
function. The epidermis is separated from the dermis by stratum compactum is composed of compactly arranged
a basement membrane of collagenous fibers. collagenous fibers. Mucous and granular (= poison) glands
The stratum corneum is sloughed (shed or molted) of epidermal origin are imbedded in the stratum spon-
periodically. The duration of the intermolt period varíes giosum, as are the scales in caecilians. Other structures
from 4—5 days in Ambystoma to 3-19 days in Bufo (Ling, in the dermis include capillaries, nerve fibers, and smooth
1972). In both salamanders and anurans, the stratum muscles.
corneum splits middorsally beginning on the head; the In salamanders and especially caecilians, there is a

Figure 14-1. Electron micrograph

of the surface layer of the epidermis
of an anuran, Phyllomedusa
sauvageí. D = desmosomes, I =
intercellular junction, M = mucoid
coat, P = protuberantes on outer
surface of epidermis, T =
tonofilaments. Bar = 1 micrometer.
Photo courtesy of R. Ruibal;
reproduced with permission from
Copeta.
 Integumentary, Sensory, and Visceral Systems
369

Figure 14-2. Photomicrograph of a

vertical section of the ventral
integument of an anuran.
Phyllomedusa sauvagei. G =
granular gland. L = lipid gland,
M = mucous gland, SC = stratum
compactum. Photo courtesy of
R. Ruibal; reproduced with
permission frorn Copeia.

practically imperceptible transition from the collagenous pipiens Ihe two types of glands and secrelory cells de-
bers of the stratum compactum of the dermis to the velop independenlly wilhoul intermedíale or Iransitional
connective tissues covering the underlying bones and types. On Ihe olher hand, McManus (1937) found Ihat
muscles. However, anurans are unique in having a loóse Ihe granular cells and glands of Desmognathus fuscus
skin attached to the body wall only at discrete places in pass through a mucoid slage during hislogenesis. During
one of the following ways: (1) by lymphatic septa which Iheir developmenl, some glands conlain bolh mucus and
are thin, transparent sheets of connective tissue that di- granular material al Ihe same time; inlermediale slages
vide the space between the skin and the muscles into could be traced from mucous to granular cells. In sludies
sepárate compartments, the lymphatic sacs; (2) by fibers of Ambystoma mexicanum and Nectophrynoides occi-
of transparent connective tissue commonly aggregated to dentalis, Le Quang Trong (1966, 1967) noled thal some
hold a particular part of the skin cióse to the body wall; glands have granular cells basally and mucous cells in or
(3) by co-ossification of the skin with underlying dermal below Ihe neck región.
bones; (4) by direct attachment of the skin to muscles, Neuwirth el al. (1979) concluded Ihat Ihe granular glands
as in the vocal sacs of some hylids (Tyler, 1971a); and are shared primitive characters among amphibians and
(5) by cutaneous muscles that inserí on the skin. T. C. Iheir original function probably was other than poison
Burlón (1980) summarized previous work on cutaneous synthesis, bul Ihe glands were a preadaplation for pro-
muscles and suggested thal two cutaneous muscles, Ihe ducing Ihe diverse loxins Ihal evolved separalely in some
m. reclus abdominis pars anleroflecla and Ihe m. cula- groups of amphibians.
neus dorsalis, may aid in Ihe adoplion of a defensive All of Ihe glands are alveolar. Typical mucous glands
poslure and in Ihe secretion of fluids from inlegumenlary are smaller man granular glands and enclosed complelely
glands in some microhylids. in Ihe stralum spongiosum (Fig. 14-2). In some salaman-
ders and anurans, Ihe mucous glands lack a distincl
Integumentary Glands. The epidermal glands myoepithelium, bul a distincl myoepilhelium is presenl
imbedded in Ihe dermis of amphibians have received in caecilians (Fox, 1983). The bases of granular glands
considerable atlenlion from morphologisls. Importanl de- may projecl inlo Ihe slralum compactum; the glands have
scriplive works on Ihe glands in salamanders are Ihose one or two types of myoepithelial cells, and al leasl in
by Dawson (1920) on Necturus, Theis (1932) on Sala- some dendrobatids there is a layer of melanophores around
mandra, and McManus (1937) on Desmognathus. Some Ihe lateral and superficial surfaces of the glands (Neuwirth
earlier workers (e.g., Muhse, 1909) believed Ihal only el al., 1979).
one kind of inlegumenlary gland was presenl in amphib- The numbers of mucous and granular glands vary
ians, even in loads. It is now known Ihal all amphibians Ihroughoul Ihe body; generally mucous glands are more
have bolh mucous and granular (= poison or serous) abundanl in Ihe dorsal skin Ihan ventrally. Interspecific
glands. dislribution of the glands, as shown in various ranids by
Conlrary views exisl on Ihe developmenl of Ihe glands. Le Quang Trong (1971, 1975a, 1975b), may be relaled
For example, Bovbjerg (1963) indicaled Ihal in Rana lo differences in habilal. Also, mucous glands are more
MORPHOLOGY
numerous and widely distributed throughout the integ- include numerous complex biogenic amines and active
ument than are granular glands, which tend to be aggre- polypeptides. Erspamer (1971) noted the presence of
gated at specific sites in many species {e.g., head and three groups of aromatic amines and five groups of poly-
neck of many anurans and some salamanders and dorsal peptides. The amines are:
surface of tail in other salamanders).
Mucopolysaccharides secreted spontaneously and 1. Indolealkylamines, including 5-hydroytryp-
continuously serve to keep the skin moist (see Chapter tamine (5-HT), which is present in most fam-
8). Granular glands secrete only following sympathetic ilies and genera of amphibians, and N- meth-
nervous or humoral stimulation. Varioussubstances (e.g., ylated derivativos such as bufotenin and
peptides and alkaloids) in these secreüons commonly are bufotenidine, which are found in pipids, lep-
noxious and in some cases híghly toxic; these secretions todactylids, bufonids, hylids, ranids, and some
are important defense mechanisms (see Chapter 10). Three salamanders.
other kinds of integumentary glands are known in am- 2. Imidazolealkylamines known from Leptodac-
phibians. Rather large, elongate glands are present in the tylus labyrinthicus and L. pentadactylus. Re-
skin in the dermal folds of caecilians; E. Taylor (1968) lated histimines occur in several unrelated
noted that these glands are associated with the dermal genera (e.g., Leptodactylus, Taudactylus, and
scales and suggested that secretions from these glands Litaría).
may form the scales. Blaylock et al. (1976) discovered 3. Hydroxyphenylalkylamines, including lepto-
lipid glands in the skin of Phyllomedusa, hylid frogs that dactylin known from various leptodactylids,
secrete an impervious coating that protects them from and epinephrine and norepinephrine known
desiccaüon (see Chapter 8). Lipid glands are slightly larger from Bufo.
than granular glands, usually are ¡n contact with the stra-
rum corneum basally, and have a distinct myoepithelium. The active polypeptides include numerous toxins (see
Breeding glands in the skin of the chest región of the Chapter 10) and other, less toxic substances:
microhylid Gastrophryne carolinensis were described by
Conaway and Metter (1967); similar glands have been 1. Eledosine-like polypeptides, such as physalae-
noted in other microhylids (see Chapter 3). The breeding min isolated from Physalaemus, phyllome-
glands are about the same size as the granular glands. dusin from Phyllomedusa, and uperolein from
The secretion is released by the fragmentation of the Uperoleia.
superficial parí of the gland, and the stícky secretion ad- 2. Bradykinin and bradykinin-like polypeptides,
heres the male to the dorsum of the female. Histochem- including bradykinin isolated from Rana tem-
ically, the secretion is similar to that of the mucous glands, poraria and phyllokinin from Phyllomedusa.
but it lacks the sulfate groups characteristic of mucus 3. Caerulein and caerulein-like polypeptides, in-
(Holloway and Dapson, 1971). cluding caerulein known from Xenopus laeuis
Clusters of mucous or granular glands form obvious and various species of Litaría and Leptodac-
integumentary structures (macroglands) in many anurans tylus, and phyllocaerulein from Phyllome-
and in some salamanders. Many of these structures de- dusa.
velop only in males in response to testicular hormones; 4. Three types of alytesin and alytesin-like poly-
these structures are present only in the breeding season peptides: I from Alytes obstetricans, II from
(see Chapter 3). The most widespread of these are nup- Bombina bambino and B. varíegata, and III
tial excrescences, which are highly keraünized clusters of from Rana pipiens.
mucous glands, on the thumbs of many kinds of anurans 5. Miscellaneous polypeptides, ¡ncluding several
and on the limbs of some salamanders. Clusters of gran- other kinds, the chemical nature of which is
ular glands may be present only in males (e.g., mental not yet known.
glands in plethodontid salamanders), and although these
glands may become enlarged during the breeding season The taxonomic distribution of many of these com-
and therefore be affected by testicular hormones, they pounds generally corresponds to the classification based
are not strictly seasonal in their presence. Other clusters on other entena, as noted for many South American anu-
of granular glands, such as the dorsal warts and parotoid rans by Cei and Erspamer (1966) and for Australo-Pap-
glands of bufonids and some salamandrids, the lumbar uan anurans by Roseghini et al. (1976) and Erspamer
glands of several genera of leptodactylids, the tibial glands (1984). Some groups of anurans (e.g., phyllomedusine
of some myobatrachids and bufonids, and the dorsolat- hylids) contain large amounts of unique polypeptides,
eral and dorsal ridges of ranids, are permanent structures. and each species has its own characteristic polypeptide
The secretions of many of these macroglands are known spectrum (Cei, 1963). The dendrobatids are well known
to be important in defense against predators (see Chapter for their strong toxins; Phyllobates produce mainly ba-
10). trachotoxins, which are extraordinarily toxic steroidal al-
The secretions produced by the integumentary glands kyloids, whereas Dendrobates secretes a variety of less
 Integumentary, Sensory, and Visceral Systems
371

Figure 14-3. A hylid frog,

Amphignathodon guentherí, from
Quebrada de Zapadores, Ecuador,
showing supraciliary processes and
calcars. Photo by W. E. Duellman.

roxic and chemically simpler piperidine alkyloids (Myers ument and noted that in many taxa, verrucae (warts) or
et al., 1978). Thus, the biochemical differences in the coni (pointed projections) have the apex covered with
genera of dendrobaüd frogs seem to have phylogenetic keratin. These structures give a roughened, sandpaper-
agnificance. Analyses of biogenic amines (Cei et al., 1972) like structure to the skin.
and secretions of the parotoid glands (B. Low, 1972) of Caecilians have dermal folds or annuli encircling or
3 ufo from throughout the world showed that trends in partly encircling the body. These annuli reflect body seg-
these biochemical traits corresponded to morphological mentation. Primary annuli overlie the vertebrae and my-
groups of toads presumably representing different evo- otomal septa, whereas secondary annuli (when present)
lutionary lineages. lie between the septa (M. Wake, 1975). The costal grooves
Too little is known about the factors affecting the bio- in salamanders also reflect body segmentation; the grooves
chemistry of granular glands to allow meaningful gener- overlie the myotomal septa and mark the position of the
alizations. For example, Myers et al. (1978) noted a de- ribs.
cline in the toxicity of secretions produced by Phyllobates Some integumentary structures, such as costal grooves
terribilis maintained in captivity. There even may be dif- in salamanders, granular ventral skin and lateral cuta-
ferences in the presence of a substance in secretions from neous channels in anurans, dermal flaps in some aquatic
glands on different parís of the body in the same species. salamanders (e.g., Cryptobranchus) and anurans (e.g.,
Serotonin was identíf ied in the secretions of parotoid glands Telmatobius culeus), and the hairlike projections on the
of Bufo alvaríus, but that compound was absent in se- flanks and hindlimbs of the aquatic ranid Trichobatrachus
cretions from the macrogland on the hindlimb (Cannon robustas, are associated with increased cutaneous vas-
et al., 1978). cularity. Increased surface área and vascularity function
to increase water uptake in terrestrial amphibians, whereas
Texture and Integumentary Structures. Although increased surface área in aquatic amphibians provides for
the skin of many amphibians appears to be smooth, usu- increased respiration (see Chapter 8).
ally it has a texture owing to various dermal and/or epi- Some kinds of integumentary structures seem to be
dermal modifications. Detailed macroscopic and histo- associated with disruptive outlines and thereby aid in
logical studies of the amphibian integument by Rabí (1931) concealment (see Chapter 10). Such structures include
and H. Elias and Shapiro (1957) have shown that the small, irregular ridges, supraciliary processes, scalloped
epidermis varíes in thickness and may have projections folds on the outer edges of limbs, and calcars (Fig.
or indentatíons, and that there are elevations and thick- 14-3). The latter are elongated triangular flaps on the
enings of various kinds in the dermis, especially in anu- heels of some anurans. The presence of calcars in many
rans. H. Elias and Shapiro (1957) provided definitions kinds of arboreal frogs living in rainforests and their ab-
and a terminology of the fine structures of anuran integ- sence in other anurans invites the speculation that they
MORPHOLOGY
372 might serve as points for runoff of water, much the same cells of the toepad are columnar, usually hexagonal in
as drip tips on leaves, or they may mimic drip típs. shape, and clearly separated from one another at their
Local thickenings of keratínized epidermis are present ápices (Fig. 14-4). The outermost surfaces of these cells
on the feet of various amphibians. The tips of the digits are fíat but covered with small, round hemidesmosome
of some stream-dwelling salamanders of the families Hy- plaques. Epidermal cells elsewhere on the digits are squa-
nobiidae, Ambystomatidae, and Plethodontidae have mous, except in an área of transition where the circum-
keratínized caps, and these are pointed and clawlike ¡n feral groove ¡s absent; in this área the cells are cuboidal.
the hynobiid Onychodacty/us japón/cus. Keratínized digit In some frogs, cuboidal epidermis also is present on the
típs are present on the forefeet of Siren. Keratínized, subartícular tubercles. Interspersed among the columnar
pointed, clawlike tips also are present on the inner three cells are mucous pores; these are numerous and bor-
toes of frogs of the genus Xenopus. The inner, and some- dered by unmodified cells in hyperoliids and rhacophor-
times outer, metatarsal tubercles of several kinds of fos- ids, and less numerous and bordered by modified cells
sorial anurans (e.g., fí/iinop/irynus, Scaphiopus) are en- in hylids. The mucous glands imbedded in the dermis
larged and covered with thick layers of keratin. are large, convoluted, and surrounded by a thin myo-
The webbing between the fingers and toes of anurans epithelium of smooth muscle. The toepads are offset from
is entírely integumentary. Webbing commonly is absent the plañe of the digit by an intercalary element between
on the hands; it is most extensive on the feet of many the distal and penultimate phalanges; this allows the en-
aquatíc frogs (e.g., pipids, Telmatobius, Pseudis, and many tire surface of the toepad to be in contact with the sub-
Rana); in these frogs the extensive webbing obviously strate. Experiments by S. Emerson and Diehl (1980) anc
provides greater surface área for the feet in propelling D. Green (1981) provided evidence that surface tensión
the animal through the water. Several arboreal anurans (capillarity) enhanced by mucous secretions is the prin-
(some species of Agalychnis, Hyla, and Rhacophorus) cipal means by which anurans adhere to smooth sur-
have fully webbed hands and feet. These frogs are ca- faces. Adhesión by toepads is supplemented by adhesión
pable of parachutíng or gliding because of the great sur- of the skin of the belly, also by surface tensión. On rough
face área present when the fingers and toes are spread surfaces, the structure of the epidermis allows interlocking
(D. Davis, 1965); one species is able to attain a gliding of the toepad with the substrate.
angle of 55° (Table 14-1). Many species of the plethodontíd salamander genus
Also related to locomotion is the grasping ability of the Boütoglossa are arboreal and have thick interdigital web-
toes of many kinds of arboreal frogs that have expanded bing and shortened digits so that the hand and foot are
adhesive toepads. Light and electrón microscopical stud- padlike with a continuous smooth margin; the epidermis
ies by Ernst (1973a, 1973b) and D. Creen (1979) have on the plantar and palmar surfaces is exceptíonally smooth.
shown that the epidermal cells in the toepads are struc- Microscopical and experimental studies by Alberch (1981)
turally different from other epidermis on the body. The and by D. Green and Alberch (1983) have shown that
toepads of arboreal frogs of the families Hylidae, Hyper- the principal mechanism of adhesión to smooth surfaces
oliidae, and Rhacophoridae are nearly hemispherical is suction created by the careful placement of the feet
structures on the ventral surfaces of the distal segments the smooth perimeters of which adhere to the substrate
of the fingers and toes. The pad is bordered, except prox- while the middle part is lifted above the substrate. The
imally, by a circumferal groove (transverse groove or cir- suction requires moisture which is provided by the mu-
cummarginal groove of some authors). The epidermal cous glands ¡n the palmar and plantar dermis.

Table 14-1. Results of Jumping Tests and Total Hindfoot Área of Gliding or Parachutíng Frogs0
Snout-vent Number of Total área of Height of Horizontal length Angle of
length (mm) triáis hindfeet (mm2) reléase (m) of jump (m) glide (degrees)
Rhacophorus otilophus
86 2 53 5.4 3.0-4.0 30-38
72 1 39 5.4 3.7 35
Rhacophorus pardalts
43 2 38 5.4 3.2 33
42 1 38 5.4 2.5 26
Rhacop/iorus nigromaculatus
89 3 221 5.4 4.8-7.3 42-55
Phrynohyas venulosa
—
— — 42.7 27.4 34
Aga/ychnis spurrelH
46-67 — — 4.5 1.5-4.0 18-41
50b — — 4.5 2.2" 23"
"Adapted from N. Scott and A. Starrett (1974).
'Median valúes.
 Integumentary, Sensory, and Visceral Systems
373

•Bpr

Figure 14-4. Scanning electrón

photomicrograph of the epidermal
surface of a toepad of Hyla
versicolor. Photo by D. B. Green.

The only other major modifications of the integument Brachycepha/us and leptodactylids of the genera Cera-
are associated with the brooding of eggs or tadpoles. The tophrys and Lepidobatmchus have large dermal plates in
dorsal pouch in hylid marsupial frogs (Gastrotheca) is the dorsal skin (Fig. 14-5). These vacularized bony shields
formed as an invagination of the integument (del Pino, are separated from the epidermis by loóse connective
1980a). In comparison with the normal skin, the lining üssue, except that rugosities on the outer surface of the
of the pouch is less keratinized and has numerous mu- shield lie adjacent to the epidermis in Brachycepha/us. In
cous glands. At the time of incubation the lining of the the latter, the plates of the shield are fused to the neural
pouch becomes highly vascularized and forms partiüons spines of the vertebrae.
between the embryos. Eggs of some other hylids (Cryp- The skin on the head is co-ossified with the dermal
tobatrachus, Hemiphractus, Stefania) are carried openly roofing elements of the skull in several groups of anurans,
on the back; mucous glands on the dorsum secrete a particularly in Bu/o and several genera of hylids. In such
matrix that forms a pad to which the eggs adhere. The cases, the stratum germinativum of the epidermis is com-
dorsal skin of female Pipa becomes thin prior to breeding; pacted. The collagenous fibers in the dermis become os-
eggs adhere to the dorsum and sink into the skin, which sified with the underlying bone, and the mucous glands
subsequently thickens and encapsulates the embryo. The and capillaries in the dermis are greatly reduced or ab-
lateral pouches in which tadpoles of Assa develop are sent, as the dermis becomes co-ossified with the under-
integumentary invaginations like those of Gastrotheca. lying bones (Trueb, 1966). Co-ossification is associated
with exostosis of the dermal bones (see Chapter 13).
Dermal Ossicles and Co-ossification. The skin of Among amphibians, caecilians are unique in that many
several kinds of anurans contains bony structures. The species have dermal scales; these are small, fíat discs set
dermis of the dorsal skin on the body of some hylid frogs in pockets in the transverse folds (= annuli). The scales
(Gastrotheca weinlandn, Phy/íomedusa bicolor, P. vail- arise in the pockets, and the basal part of each scale is
lanti) contains small, vascularized bony plates (osteo- attached to connective üssue in the deep part of the pocket.
derms) from which bony lamellar spines protrude into The scales have three principal layers. The basal layer is
the epidermis. The pelobatid Megophrys nasuta and the cellular. The middle portón is composed of bundles of
leptodactylid Hylactophryne augusti have avascular os- parallel collagenous fibers arranged in two or three layers
teoderms composed of calcified bundles of collagen. In of different orientations. The superficial layer consists of
all of these frogs the collagen fibers of the stratum com- mineralized squamulae separated from one another by
pactum often are continuous with the ossified lower sur- concentric and radial furrows lacking mineralizatíon. The
face of the osteoderms (Ruibal and Shoemaker, 1984). most superficial of the fibrous layers is unmineralized and
MORPHOLOGY
374

Figure 14-5. Brachyccphalus

ephippium. A. Dorsal view of cleared
and stained adult (snout-vent length
16 mm) showing hyperossification of
skull and presente of a broad dermal
píate overlying vertebral column.
B. Transverso cross section of
midbody vertebra showing fusión of
dermal spine with overlying dermal
shield. Bones are black. Photos by
L. Trueb.

is contiguous with the mineralized squamulae; mineral absent in scolecomorphids and some caeciliids, both of
deposits are present on those fibers that extend into the which are fossorial.
squamulae (Zylberberg et al., 1980).
E. Taylor (1972) provided an atlas of caecilian scales Chromatophores and Pigmentation
in which he noted that the patterns of concentric and The chromatophores and pigments in amphibians have
radial furrows were different among taxa. The question been studied extensively, particularly by Bagnara and his
of independen! origin of caecilian scales versus homology associates—Bagnara and Ferris (1971), Bagnara and
with osteichthyan scales is unresolved (see Zylberberg et Hadley (1969, 1973), Bagnara et al. (1969, 1973, 1978,
al., 1980, for discussion). Although the scales may pro- 1979), Hadley and Bagnara (1969), S. Frost and Bag-
vide some protection, the large number of scales ar- nara (1979a, 1979b), and S. Frost and S. Robinson
ranged in specific circular and overlapping repetitive pat- (1984). The synthesis that follows is derived primarily
terns along the body and associated with the musculature from these works.
may have a role in locomotion by providing requisite
rigidity while pcrmitting a wide range of body move- Structure and Function. Amphibian chromato-
ments. Such a function might explain their usual absence phores are located in either the epidermis or dermis. Me-
in the aquatic typhlonectids, but scales also appear to be lanophores are the predominant type of epidermal chro-
 Integumentary, Sensory, and Visceral Systems
Tatophores, although erythrophores have been observed tenoids in discrete pigment organelles (Fig. 14-7A). Such 375
r. :he epidermis of some amphibians (e.g., Notophthal- cells are best termed xantho-erythrophores.
—.us uiridescens, Forbes et al., 1973). Epidermal melan- Iridophores underlie xanthophores; these cells (also
ophores are thin, elongate cells with long dendritic called guanophores) are white or silvery in appearance
processes that extend between surrounding cells. For ex- and have the capacity to reflect light of specific wave-
ample, in tadpoles of Bombina orientalis, epidermal me- lengths through the overlying xanthophores. Together,
¿r.ophores form an elabórate orthogonal network com- the xanthophores and iridophores interact to produce
oosed of melanophores each with four dendritic processes bright colors. Iridophores reflect light by virtue of the
radiating symmetrically from a central cell body (Ellinger, arrangement of their pigment-containing organelles (i.e.,
1980). Epidermal melanophores are characteristic of lar- reflecting platelets). These organelles commonly are ar-
val amphibians; upon metamorphosis these may be lost ranged in parallel stacks which thus function as a multi-
DÍ their number reduced as the dermis thickens and der- layer interference reflector (i.e., a "mirror," S. Frost and
—,al chromatophores develop. Epidermal melanophores, S. Robinson, 1984). The principal pigments in these cells
ike those in the dermis, produce pigments known as are purines (e.g., guanine, hypoxanthine, adenine).
eumelanins, which are deposited within organelles known Often, the iridophore layer in amphibian skin is only
as melanosomes. An epidermal melanophore unit con- one cell layer thick. An exceptíon occurs in the arid-adapted
ssts of a melanophore and surrounding epidermal cells species of African rhacophorid frogs, Chiromantis, which
Malpíghian cells) that act as receptors of melanin do- have chromatophore units containing 3—5 layers of
r-.ated by the melanophores through cytocrine activity. iridophores; presumably this results in increased reflec-
In the dermis of most amphibians that have been stud- tance, which might be correlated with reducing evapo-
:ed there usually are three types of chromatophores that rative water loss (Drewes et al., 1977). In a blue morph
are arranged in what has been termed a dermal chro- of Dendrobates puntillo, xanthophores are lacking and
matophore unit (Fig. 14-6). In this unit, xanthophores (or iridophores are stacked in layers above the underlying
erythrophores) are the most superficial cells; they lie just melanophores (Fig. 14-7B; S. Frost, unpubl. data). In this
relow the basement membrane separating the epidermis case the iridophores reflect blue light, which, in the ab-
I
and dermis. Xanthophores impart yellow, orange, or red
colors primarily because of the presence of pteridine pig-
sence of overlying red or yellow pigments, imparts a
structural blue color to the skin.
ments. In some cases the red, yellow, or orange colors Melanophores are the basal-most chromatophores;
observed in amphibian skin are caused by the presence dendritic processes extend upward to termínate on the
of carotenoid pigments that are concentrated in carote- upper surfaces of iridophores, between these cells and
noid vesicles in cells best described as erythrophores. the overlying xanthophores. The principal pigment of
Some anurans, such as Bombina orientalis, have dermal melanophores is eumelanin. In phyllomedusine
chromatophores that contain both pteridines and caro- and some pelodryadine hylids (Bagnara and Ferris, 1975;

epidermis—

basement membrane

'xanthophore

iridophore

melanophore

Figure 14-6. Diagrammatic

representation of dermal
chromatophore unit in a dark phase.
Photo courtesy J. T. Bagnara.
MORPHOLOGY
376 Tyler and M. Davies, 1978b), melanosomes are ex- enoid which appears red-orange. Thus, differences in lo-
tremely large and contain, in addition to a eumelanin cation and composition of chromatophores result in the
core, a red pigment, pterorhodin, which is a pteridine different colors and patterns observed in amphibians (see
dimer. This pigment and unusual type of melanosome reflectance model of Nielsen and Dyck, 1978).
are unknown in other vertebrales (Misuraca et al., 1977). In addition to the presumably genetically based color
Characteristically in adult amphibians, the dermal dimorphism observed in many species of amphibians,
chromatophore unit responds to physiological changes there are occasional examples in nature of melanism and
by affecting a change in color, usually manifested as a albinism (Dyrkacz, 1981). The genetic basis for the color
darkening or lightening of the skin. It is only when dermal variants has been studied in species of ñaña and in the
chromatophore units contain two or more chromato- axolotl, Ambysíoma mexicanum (C. Richards and Nace,
phore types, with melanophores residing deepest within 1983; S. Frost et al., 1984, andreferencestherein). Peculiar
the unit, that color changes are affected. blue variants are known in R. catesbeiana and R. clam-
In amphibians, blue skin is primarily a structural phe- itans. The problem in these frogs seems to reside in the
nomenon resulting from both the reflectíng and scattering xanthophores, which have abnormal pterinosomes and
(i.e., Tyndall scattering) propertíes of iridophores and the lack bright-colored pteridine pigments (Bagnara et al.,
absence of xanthophores or bright-colored xanthophore 1978).
pigments. When yellow pigments are present in the xan- Bagnara, Matsumoto et al. (1979) proposed that the
thophore layer, the pigments act as filters such that blue different chromatophore types are derived from a com-
light reflected from the underlying iridophores and pass- mon stem cell containing a primordial organelle. Cues
ing through the yellow layer will appear green. This, in present in the tissue milieu díctate the fate of this orga-
fact, is the basis for the observed green skin color of many nelle. Thus, differentiation of the stem cell into a specific
amphibians, although shades and intensity of green colors chromatophore may be controlled genetically, hormon-
may vary tremendously. ally, or environmentally. Developmentally, pigmentary
According to S. Frost and S. Robinson (1984), there changes may occur at various stages in the life cycle.
are three major factors contributing to green color in frog C. Richards (1982) determined that chromatophore pig-
skin: (1) the kind of yellow pigment (i.e., carotenoids or ments change ontogenetically with the development of
pteridines) in xanthophores, (2) the quantity of yellow sex hormones in the African treefrog Hypero/ius viridifla-
pigment in xanthophores, and (3) the arrangement of vus. During and subsequent to metamorphosis, the ma-
pigment organdíes in the iridophores below the xan- jority of pterinosomes in xanthophores are replaced by
thophores. The first two factors presumably account for carotenoid vesicles in the dorsal skin of Bombina orien-
differences in the intensity of green color, whereas the talis (S. Frost and S. Robinson, 1984) and Notophthal-
last probably affects the quality (shade or tone) of green. mus uirídescens (Forbes et al., 1973). Thus, the chro-
In their studies of Bombina oríentalis, these investigators matophores and pigment compositions of the amphibian
noted that the structural arrangement of reflecting plate- integument represent a highly dynamic system.
lets in the green dorsal skin is such that these organelles
function as refractosomes (i.e., multiple-layer interference Color Change. Two kinds of color change can be
reflectors). Furthermore, the red color on the venter of affected by the chromatophore units of amphibians. Rapid
Bombina is explained easily because ventral skin lacks color changes involving intracellular mobilization of pig-
iridophores, only a few melanophores are present, and ment-containing organelles are referred to as physiolog-
the xanthophores contain only carotenoid vesicles. The ical color changes; this change results from hormonal
pigment in these vesicles ¡s densely concentrated carot- stimulatíon. These changes may require only seconds to

Figure 14-7. Photomicrographs of

amphibian chromatophores.
A. Epidermal melanophore pattern in
dorsal skin of a tadpole of Bombina
orientalis. The melanophores form a
highly organized, reticulate network
within the epidermis. Bar = 25 |im.
B. Stacked ¡ridophores in the dermis
of Dendrobatos pumilio. The skin of
this specimen was a deep blue-black.
Two layers of reflecting pigment cells
(iridophores) are located immediately
below the epidermis. Melanophores
lie beneath the iridophore layer.
Abbreviations: E = epidermal cell,
I = iridophore, M = melanophore
«i
í
process. Bar = 1 (jim. Photos by
S. K. Frost. I "*"
 Integumentary, Sensory, and Visceral Systems
accomplish and commonly are of short duration (minutes surface to being irregular, and (3) xanthophores change 377
to hours). Color changes that are evoked slowly and that from a lens shape to a píate shape. During intermedíate
involve the accumulation or reduction of the amount of darker stages, xanthophores migrate down between irid-
rigment are referred to as morphological color changes. ophores and may even go beneath iridophores; the pter-
This is a slow process because it involves the synthesis inosomes gather in the periphery of the cell, and carot-
or destruction of relatively large amounts of pigment as enoid vesicles aggregate around the nucleus.
a result of either the persistence or continuous lack of Color change in adult amphibians seems to be mostly,
snmulation of the chromatophores. Such changes are of if not exclusively, controlled by circulating levéis of MSH
long-term duration (days to months). which disperses melanosomes in melanophores and causes
Epidermal melanophores undergo morphological aggregation of reflecting platelets within iridophores and
changes. Some anurans subjected to continuous stimu- dispersión of pigmentary organelles in some xantho-
iation deposit so much melanin in adjacent epidermal phores. The secretion of MSH is under inhibitory regu-
cells that practically the entire epidermis becomes melan- lation, possibly by the hypothalamus. Electrophysiologi-
ized. Within the dermal melanophore unit, increases in cal studies by Oshima and Gorbman (1969) indicated
melanin may be accompanied by a decrease in guanine the presence of two types of active electrical units in the
in iridophores. Thus, the morphological effects elicited by pars intermedia of anurans; one of these neurons is in-
iridophores and melanophores are supplemental to one hibited by light, and the other is indifferent to illumina-
another. tion. Thus, it was proposed that these two nervous ele-
Morphological color changes usually are preceded by ments are in balance and regulated by the influence of
physiological color changes, but morphological color light on one of them. The light-inhibitable neuron is con-
change is not a necessary consequence of physiological sidered to stimulate the reléase of MSH under conditions
color change. Morphological color change involving an of low illumination.
increase in the amount of pigment contained in a chro- Amphibian larvae become palé when subjected to pro-
matophore seems to be related to the dispersión of the longed darkness; the melanosomes aggregate in the mid-
pigment-containing organelles in the cell, just as a de- dle of the melanophores. Experiments by Bagnara (1960)
crease in pigment content is accompanied by an aggre- revealed that this change was negated by pinealectomy,
gation of the organelles in the middle of the cell. The but administration of pineal hormones induced the ag-
occurrence of morphological color change in the absence gregation of melanosomes. The hormone melatonin, se-
of physiological change was noted by J. D. Taylor (1969) creted by the pineal gland, is a melanosome-aggregating
for Hy/a cinérea; when the frogs were treated with MSH agent. The reléase of melatonin is regulated by light re-
(melanocyte-stimulating hormone; intermedin) there was ceptors in the pineal body.
dimunition of purines in the iridophores, but the orga- Controversy exists whether color change in adult am-
nelles remained aggregated. phibians is caused solely by levéis of MSH or involves
Physiological color changes in the dermal chromato- other hormones. In vitro. the contraction of iridophores
phore unit involve the dispersión and aggregation of mel- by MSH can be counteracted by the administration of
anosomes and reflecting platelets. In a palé color phase, norepinephrine or acetylcholine (Bagnara et al., 1969).
melanosomes are aggregated in a perinuclear position, Nielsen and Dyck (1978) observed differential dispersión
and the melanophores contribute little to the color of the of organelles in the three types of chromatophores in
animal. Concomitantly, the iridophores are not obscured Hy/a cinérea and concluded that MSH could not be the
by overlying melanin and the reflecting platelets are fully only agent influencing color changes; they did not rule
dispersed (in those iridophores that show physiological out the possibility of nervous control of the chromato-
color change). Xanthophores, which apparently do not phores, as did Bagnara and Hadley (1973). Moreover,
undergo cellular rearrangement during physiological color chromatophores may be sensitive to light, as shown in
change, play only a passive role by serving as a yellow Pachymedusa dacnicolor by Iga and Bagnara (1975).
filter. Thus, the net effect of these iridophore and melan- Observatíons on numerous kinds of amphibians indí-
ophore responses is that the animal becomes paler in cate that color change can be affected by changes in
color. In a dark color phase, there is an aggregation of illumination and also by temperature. Moreover, in at
iridophore pigments thereby reducing the reflecting sur- least some species color change is affected by back-
face área and a dispersión of melanosomes into the mel- ground color; the animáis become darker on dark back-
anophore projections that cover the iridophores. grounds. However, this is not a generality. For example,
Nielsen's (1978a) ultrastructural studies of color change Nielsen (1979) experimented with two color phases of
in Hy/a arbórea also demonstrated that during the change Rana escalenta; the green color phase changed in re-
from a palé to dark color phase: (1) dermal melanophore sponse to a palé background, whereas the brown phase
projections partly surround the xanthophores as well as did not. Experiments with Hy/a arbórea and H. cinérea
the iridophores, (2) iridophores change from a cup shape by Nielsen (1978b) revealed that both species became
to a cylindrical or conical shape, with a simultaneous palé when treated with epinephrine; also, stress (frogs
reorientation of platelets from being parallel to the upper pressed into a plástic box) affected the hue and purity of
MORPHOLOGY
378 the dorsal color of H. arbórea and the paleness of mitted to the brain so that the organism may respond
H. cinérea. appropriately.
The dilemma expressed by Bagnara and Hadley
(1973:74) remains unresolved: ". . . chromatophores may Lateral-line System. The lateral-line system is a col-
be affected by either hormonal or neurohormonal agents lection of epidermal sense organs distributed over the
as well as by direct environmental influences. . . . Certain head and along the body in aquatic amphibians. Lateral-
hormones may be inhibited from being released under line organs are present in aquatic larvae, aquatic adult
condiüons of illumination, whereas others may bevre- salamanders (e.g., Cryptobranchus, Necturus, Am-
leased under conditions of darkness, or vice versa. In phiuma, and Siren), adult pipid frogs, and adult sala-
either situation the chromatíc responsos may appear sim- mandrids that are aquatic after a terrestrial stage (e.g..
ilar, although their regulatory basis may be quite differ- Notophthalmus) or remain aquatic (e.g., Neurergus).
ent." The biology of lateral-line receptors in salamanders and
anurans was reviewed by Russell (1976) and in caecilians
Integumentary Sensory Receptors by Hetherington and M. Wake (1979). Also, new infor-
As the interface between the organism and its environ- mation was provided on salamanders (Neurergus) by
ment, the integument receives stimuli that must be trans- Gorgees et al. (1977). Earlier work on the lateral-line
system involved only the identification of mechanorecep-
tors, the neuromasts. The identification of ampullary or-
gans that are electroreceptors has been more recent—
-supraorbit al -supraspiracular Hetherington and M. Wake (1979), Fritzsch (1981), Münz
-inf -aorbital body-. et al. (1982), Himstedt et al. (1982), and Fritzsch and
-postorbital Wahnschaffe (1983).
The structure and arrangement of the lateral-line or-
; gans (neuromasts) are similar in different amphibians.
The organs are distributed singly (Siren) or in small groups
along the lateral or dorsolateral surface of the body and
especially on the head, where distinct patterns are evi-
dent on dorsal, lateral, and ventral surfaces (Fig. 14-8).
Each neuromast consists of a pear-shaped group of
Lora I guiar- cells imbedded in the epidermis and resting on the base-
Lmandibular spiracular-1
ment membrane. Each organ is constructed of three types
B rinfraorbital body of cells: (1) mantle cells forming the periphery, (2) sup-
r nasal porting cells infernal to the mantle cells and extending
from the basement membrane to the surface, and (3)
sensory cells or hair cells in the apical half of the organ.
The organs protrude beyond the surface of the skin in
larvae but usually are recessed in a small pit in adults
The apical surface supports a thin, ribbonlike projectíon.
the cúpula. On the apical end of each sensory cell is a
single, long kinocilium and a group of much shorter
supraorbital supraspiracular steriocilia, which decrease in length with increasing dis-
tance from the kinocilium (Fíg. 14-9). Neuromasts are
innervated by one efferent and two afferent nerve fibers.
guiar
-infraorbital Most neuromasts on the head are innervated by the an-
terior lateral-line nerve (lateralis anterior of C.N. VII), and
all remaining neuromasts by the posterior lateral-line nerve
(lateralis posterior of C.N. X). Fibers from these two nerves
enter the área of the acousticolateralis in the dorsolateral
wall of the medulla.
In Notophthalmus virídescens the neuromasts are nor-
mal during the aquatic larval and adult stages, but during
the subadult terrestrial stage the cells in the neuromasts
-oral dedifferentiate until they are alike cytogenetically (Daw-
Lmandibular
son, 1936). In the adult aquatic stage, the sensory cells
are replicated by división of both sensory and supportíng
Figure 14-8. Distribution of lateral-line organs in ¡chthyophis. cells. It is not known if there are changes in the nerve
A. Lateral. B. Dorsal. C. Ventral. Open structures are neuromasts;
solid structures are ampullary organs. Redrawn from Hetherington fibers innervatíng the neuromasts of Notophthalmus, but
and M. Wake (1979). in the terrestrial stage of Tríturus cristatus, which under-
 Integumentary, Sensory, and Visceral Systems
379

=~e'ent fiber J -sensory cell afferentfibers-1 -sensory cell

Figure 14-9. Comparative structure of
A. ampullary organs and B. neuromasts ¡n
Trituras alpestris. Redrawn from Fritzsch and
efferent fiber- Wahnschaffe (1983).

; similar dedifferentíation of neuromast cells, the nerves and associated structures receive olfactory signáis, and
jegenerate (Russell, 1976). Some neuromasts in aesti- the ears receive acoustic signáis and vibrations. The pin-
.2±p.g Siren intermedia dedifferentiate and sensory cells eal organ also is a photoreceptor. The morphology and
kxtse the cilia, as they are overgrown by epidermis (Reno function of each of these systems are discussed in this
a-.c Middleton, 1973). sectíon; the integumentary receptors, including the lat-
Ampullary organs are present in larval caecilians and eral-line system, are discussed in the foregoing section:
acuatic salamanders; there is no trace of these organs in Integument.
ar.-jrans or in plethodontid salamanders that undergo di-
ré- development. The ampullary organs are restricted to Visual System
rve head, where they are less numerous than neuromasts The eyes of terrestrial amphibians show numerous ad-
ru: commonly are associated in parallel fashion with rows vances over those of fishes. The lens is flattened and it
3 r.euromasts. The ampullary organs are like neuromasts lies behind the iris; muscles of accommodation are present,
r. general structure except that they are sunken in the and protectíve lids and glands are present in terrestrial
epidermis, lack a cúpula, have a long neck, and have forms. The eyes of amphibians, especially those of anu-
rscuced capillarity. Moreover, ampullary organs have one rans, have been studied morphologically and electro-
¿usier of microvilli per sensory cell and no kinocilium or physiologically (Walls, 1942; Fite, 1976).
seriocilia, and they have only one afferent nerve fiber
2--.¿ no efferent nerve fibers. Hetherington and M. Wake Structure. The eyes of living amphibians vary greatly
1979) suggested that ampullary organs are derived from in size. Those of terrestrial and arbórea! anurans and
sunken neuromasts. terrestrial salamanders, especially plethodontids, are pro-
Neuromasts function as mechanoreceptors; they are portionately largest, whereas those of aquatic and fos-
sensitive to water currents and probably also to pressure sorial species are smaller; the eyes of subterranean sal-
Russell, 1976). Ampullary organs are electroreceptors amanders and caecilians are very small. In the case of
Münz et al., 1982). salamanders (Proíeus, Haideotriton, Typhlomolge, Ty-
phlotriton, and one species of Gyrinophi/us), the eye
Other Integumentary Receptors. The dermis con- undergoes normal development untíl a certain stage when
2ir.s many unmyelinated nerve fibers, and some of these growth and differentiation cease and degeneration begins
axons extend into the epidermis. Investigations of these (Schlampp, 1892; Eigenmann, 1900; Brandon, 1968;
receptors were summarized by Cartón (1976) and Spray Besharse and Brandon, 1973,1974). In the case of some
11976). The free nerve endings are thought to be the small species of terrestrial salamanders (e.g., Thoríus and
ransduction elements for various stimuli. Various exper- Batrachoseps), miniaturization has been achieved by re-
mental studies indícate that cold and heat receptors and duction or loss of cranial elements, accompanied by a
actué receptors are located in the epidermis, whereas relative increase in the size of the sense organs (G. Roth
oain receptors and pressure receptors are situated in the et al., 1983).
dermis. The eyeball is nearly spherical. Distally the eyeball is
covered by a transparent membrane, the cornea (Fig.
14-10A). The remainder is covered by a dense fibrous
SENSORY RECEPTOR SYSTEMS layer, the sclera, which is strengthened by a cup or ring
As in all terrestrial vertebrales, three major sensory re- of cartílage in anurans, most larval salamanders, and adults
ceptor systems are present in amphibians. The eye and of paedomorphic salamanders. The scleral cartílage is
its associated structures receive visual signáis; the nares greatly hypertrophied in crytobranchid salamanders, in
MORPHOLOGY
380
upper eyelid

m protractor
lentis

pupillary
optic nerve nodule

sclera
nictitating
membrane

lower eyelid

ciliary process
iris
m protractor lentis

cornea
zonule fibers

cüiary epithelium
m ciliaris
Figure 14-10. Semidiagrammatic views of the retina
eye of Rana pipiens. A. Cross section of eye.
B. Ventral ciliary process and associated sclera
structures. Adapted from Walls (1942).

some terrestrial salamanders (e.g., Ambystoma), and in folded again partly by protrusion of the eyeball but chiefly
the microhylid frog Stereocyc/ops incrassatus (Walls, 1942). by a slip of the m. levator bulbi which inserís on the
In most salamanders and anurans, eyelids develop at ventral side of the posterior end of the lower eyelid. Eye-
metamorphosis; they are absent in oblígate neotenic sal- lids are absent in caecilians, in which the eye is covered
amanders and in pipid frogs. The upper eyelid is merely by translucent skin, undifferentiated skin, or bone.
an integumentary fold with limited independen! move- The orbital glands that lubrícate the eye are present
ment. The lower eyelid is much more movable and is along the length of the lower eyelid in primitive sala-
variously modified in some salamanders and many anu- manders. Numerous ducts open onto the conjunctiva.
rans. According to Noble (1931b), the upper parí of the the mucous membrane that lines the eyelids and extends
lower eyelid is thin, translucent, and folded on itself to onto the sclera of the eyeball. In some salamanders (e.g..
form an N-shaped structure; the translucent upper por- Salamandra), the glandular tissue is differentiated into an
tion is the nictitating membrane. It arises from a small anterior Harderian gland and a posterior lacrimal gland.
mass of undifferentiated tissue at the anterior córner of Only the anterior (Harderian) gland is present in anurans
the eye in larvae. In some anurans (e.g., Agafychnis and and caecilians. The Harderian gland is greatly hypertro-
Nyctimysíes), both parts of the lower eyelid are translu- phied and occupies most of the orbit in caecilians; its
cent or even transparent with a pigmented reticulated secretions lubrícate the tentacle. The lacrimal duct leads
pattern. A tendón that encircles the eyeball is attached from the orbit to the nasal chamber; in salamanders the
to either end of the upper edge of the nictitating mem- duct opens on the conjunctiva near the anterior córner
brane. When the eyeball is retracted into the orbit, the of the eye, whereas it opens on the middle of the lower
tendón draws the membrane up over the cornea. The eyelid in anurans.
nictitating membrane is withdrawn and the lower lid is The lens is large and flattened; it is more nearly spher-
 Integumentary, Sensory, and Visceral Systems
ical in oblígate neotenic salamanders, and it is clouded outer segments. The presence of two kinds of rods is 381
in caecilians. The chorioid coat is thinner in anurans than unique to amphibians, the only group to possess green
in salamanders, and it is pigmented (xanthophores and rods. However, green rods are absent in caecilians and
iridophores) in both groups. In caecilians, the chorioid in some subterranean and oblígate neotenic salaman-
coat is thinner than in anurans and lacks pigment. The ders. Red rods maximally absorb wavelengths of 502 nm
ciliary body is largest and most complex in anurans. The and have long outer segments and short myoids. Green
body is roughly triangular (Fig. 14-10B). The zonule área rods maximally absorb wavelengths of 432 nm and have
is formed by crescentric fibers of the ciliary muscles. These short outer segments and long, thin myoids (Fig. 14-11).
fibers suspend the lens. Accommodation is accomplished Cones are single or double. Single and primary members
by protraction of the lens by the protractor lentis muscles. of double cones maximally absorb wavelengths of 580
One large ciliary fold (= ciliary process) is present mid- nm, and the smaller accessory members of the double
ventrally, and there are two or three large folds dorsally. cones maximally absorb wavelengths of 502 nm. The
The ciliary bodies are smaller in salamanders, and ciliary nuclei of the rods lie next to the outer limiting membrane,
muscles usually are present dorsally and ventrally; only whereas the nuclei of the cones are more proximal to the
a midventral ciliary fold is present. Caecilians lack ciliary outer nuclear layer. Both kinds of rods and cones show
bodies and have no means of accommodaüon. marked photomechanical movements, except that ac-
The iris surrounds the lens; it is pigmented, and it can cessory cones are immobile.
be dilatad or contracted to control the size of the pupil Electron microscopic studies by Nilsson (1964) re-
and thus the amount of light that strikes the retina. The
iris consists of two retínal layers and one stroma layer in
salamanders and anurans. The epithelial layers are pig-
mented; both iridophores and melanophores are present,
and in some anurans xanthophores also are present. The
irises of salamanders and some anurans are black or dull
brown, but those of many anurans are brilliantly colored
or have a concealing coloration blending in with the facial
color pattern. Thus, many species of Rana and Eleuth-
erodacíy/us, as examples, have a dark streak through the
eye that is conünuous with a stripe of the same color
extending from the snout at least to the posterior end of
the head. Many anurans (e.g., someHy/a and Bufo) have
brilliant gold reticulaüons on the iris, and other hylids
(e.g., Agalychnis and some Hyla) have a bright uniform
red or orange iris, and some Phyllomedusa have a palé
silvery-gray iris. In caecilians, the iris consists of only two
epithelial layers, only one of which contains pigment.
Dilation and contractíon of the iris is accomplished in
salamanders and anurans by actíons of the mm. dilatator
pupillae and sphincter pupillae, respecüvely. In anurans
with a horizontal pupil, contractíon is correlated with the
presence of large dorsal and ventral pupillary nodules;
these nodules are absent in salamanders. Salamanders
have round pupillary apertures, but the shape is variable
among anurans—round, triangluar, vertícally elliptícal, or
horizontal. These shapes have some systematic consist-
ency (see Chapter 17), but the differences in the patterns
of músete fibers have not been investigated.
The vast amount of information on the retina in am-
phibians was summarized by Dowling (1976), J. Cordón
and Hood (1976), and Grüsser-Cornhels and Himstedt
(1976). The retina is a thin, complex structure consisting
Red rod Green rod
of five layers: (1) pigment epithelium, (2) outer nuclear (502) (432)
layer containing receptor nuclei, (3) outer plexiform layer, Single cone-1 Accessory Principal
(4) inner nuclear layer containing nuclei of horizontal, (580) (502) (580)
bipolar, and amacrine cells, and (5) inner plexiform layer.
There are four types of receptors in amphibians. These Figure 14-11. Schematic drawing based on an electrón
micrograph of the receptor layer in the retina of Rana pipiens.
consist of two kinds of rods and two types of cones, Numbers in parentheses are peak sensitiuities (nanometers).
receptor cells so designated because of the shapes of their Adapted from Nilsson (1964).
MORPHOLOGY
382 vealed that the outer segments of the rods are made up during metamorphosis (see Chapter 7). However, in at
of a series of discs that are stacked vertically within the least one species, Rana catesbeiana, the retina in adults
plasma membrane. These discs originate as invaginations contains as much as 30-40% porphyropsin, all of it con-
at the base of the outer segment; subsequently, the discs centrated in the upper third of the retina (Reuter et al.,
are pinched off and become separated from the plasma 1971). In this species which commonly sits in water with
membrane. The outer segments of cones are made up only the upper half of the eye above water, the upper
of a stack of discs of decreasing diameter, but cones differ part of the retina receives images from below the water
from rods in that the discs are a series of invaginations and the lower part receives images from above the water.
of the plasma membrane. In rods, new discs are formed
continuously at the base of the outer segment; the discs Perception. Vision plays an importan! role in environ-
move up the outer segment until they finally detach ter- mental sensing in anurans and most salamanders. The
minally and are absorbed by the pigment epithelium. degenerate eyes of caecilians and subterranean salaman-
Shedding of the terminal discs is synchronous in about ders allow them to distinguish between light and dark at
25% of the rods daily; shedding occurs with the onset of best, and in those taxa in which the optíc nerves have
light (Basinger et al., 1976). Thus, rods constantly are no connectíon with the eye, obviously no signáis are
renewing themselves, but cones do not renew themselves transmitted to the brain, so the eyes do not have a sen-
in this manner. sory function. Various behavioral and neurophysiological
The outer segments of all receptors are attached to studies have provided importan! data on visual percep-
their inner segments by a thin cilium. The inner and outer tíon in anurans and salamanders.
segments intedigitate with long strands from the pigment Light intensity and spectral sensitivity.—Classically.
epithelial cells. The inner segments of single cones and animáis have been classified as photopositive or photo-
principal members of double cones contain an oil droplet negative. Furthermore, amphibians generally have been
in their ellipsoids that is essentially transparent to visible considered to lack color visión. Muntz (1962) showed
light. The numbers of different kinds of rods and cones that Rana temporaria was photopositíve to white light
vary in relatíon to the amount of light to which the species intensitíes and responded to blue light. The same results
normally is exposed. In Rana pipieos, the proportíon of were obtained for Triturus cristatus (Muntz, 1963a), but
different receptors is: green rods 8%, red rods 50%, sin- Salamandra salamandra was photonegatíve to white light
gle cones 18%, principal members of double cones 12%, intensitíes and responded strongly to the two ends of the
and accessory members of double cones 12% (Lieb- visual spectrum (a U-shaped spectral response peaking
mann and Entine, 1968). in red or violet).
The outer plexiform layer contains the receptor ter- In a series of experiments on 121 species of anurans.
mináis; behind this layer is the inner nuclear layer con- Hailman and R. Jaeger (1976, and other papers cited
taining three kinds of cells and synapses. Processes of therein) showed that each species has a preferred white
bipolar cells ramify in the outer plexiform layer and syn- light intensity (optimal ambient illumination) to which it
apse with the receptors; others extend into the inner plex- responds phototactically. Most species prefer illuminance
iform layer. The horizontal cells lie distally ¡n the inner above 90 lux, a few less than 0.01 lux, and the rest
nuclear layer; the processes of these cells extend laterally between these valúes. Hailman and R. Jaeger suggested
in the outer plexiform layer and end in the vicinity of the that the response to blue light is based on true color
receptor termináis. The amacrine cells are proximal in visión, but that the U-shaped spectral response probably
the inner nuclear layer; their processes end in the inner is a function of spectral selectivity. They proposed the
plexiform layer, which is thicker and more complex than following relationship between responses by anurans to
the outer plexiform layer. It is the región where bipolar intensity and spectral cues: (1) When the ambient illu-
cells and amacrine cells synapse with ganglion cells from mination is brighter than the optimal ambient illumination
the optíc fibers. for a given species, the individual responds photonega-
tively and exhibits the U-shaped spectral response, be-
Pigments. The principal visual pigment in terrestrial cause the ends of the visible spectrum appear dimmest
amphibians is the red-photosensitive rhodopsin con- to the eyes. (2) When ambient light is dimmer than the
tained in the red rods. The same pigment ¡s present in optimal ambient illumination, the individual responds
cones but the absorption peak is 580 nm in single cones photopositívely and exhibits the blue response based on
and principal members of double cones versus 502 nm true color visión. (3) When ambient light is at the optimal
in red rods and accessory members of double cones. The level, the individual attempts to maintain that intensity
lower absorption peak of 432 nm in green rods suggests and is indifferent to colors. This model proposes that
that green rods have a yellow pigment (Donner and Reu- phototaxis is merely a means by which anurans of dif-
ter, 1976). ferent species seek the ambient illumination that is opti-
The visual pigment in larval amphibians and those that mal for their visual system.
remain aquatic as adults is the purple-photosensitive por- The experiments by Hailman and R. Jaeger indícate
phyropsin. The change in visual pigments takes place that phototactic behavior is associated with four related
 Integumentary, Sensory, and Visceral Systems
-- .T.r.ogical mechanisms which contribute to the diver- iations in objecl dislance (Grüsser and Grüsser-Cornhels, 383
9^" of behavioral responses to light of different intensities 1976).
anc wavelenglhs: (1) possession of different kinds of Pattern discrimination.—Letlvin el al. (1959) dem-
-•- ::::eceptors having different absorption levéis, (2) onslraled Ihal Ihe outpul of Ihe retina in anurans is com-
pupLary responses that control the amount of light posed of four facete of Ihe visual images: (1) local sharp
-;-i;-.-.- rhe retina, (3) migration of pigment epithelium edges and conlrasl, (2) movemenl of edges, (3) local
:: - r: ..:ng the amount of light striking individual receptor dimmings produced by movemenl or general rapid dark-
cefc. and (4) dark- and light-adaptation of photoreceptor ening, and (4) Ihe curvalure or Ihe edge of a dark objecl.
.-«*= which increase sensitivity in darkness and increase The fibers involved respond besl when an object smaller
x in bght. Ihan Ihe receptive field enlers Ihe field, stops, and moves
Himstedt's (1972) experimenta on selection of colored aboul. The response is nol affecled by changes in lighting
prey dummies by Salamandra and Trituras indícate that or by moving Ihe background. Thus, Ihe eyes of am-
±ese salamanders exhibit a U-shaped spectral response phibians are excellenl al visually isolating polential prey
üke that reported for anurans by Hailman and R. Jaeger of a corred size.
1974). All experimental evidence indícales at least a lim- Experimente! work on anurans summarized by Ingle
::ed distinction of different wavelengths of light, but so (1976) and Ewert (1976) was expanded by Ingle and
far there is no solid evidence for the ability to perceive McKinley (1978), Ewert el al. (1978), and Burghagen
the differences in colors evident in so many species of and Ewert (1983). Experimente were performed on sal-
anurans or the breeding coloration in male newts (Tri- amanders by G. Rolh (1978), Lulhardl and G. Rolh
turus). (1979), and Finkensládl and Ewert (1983). Sludies on
The presence of different photopigments in the retinas loads show thal elongation of Ihe prey along Ihe axis of
of larval amphibians presumably is the primary factor for movemenl facilitates caplure; Ihere is a slronger effecl for
tadpoles responding to green light instead of blue light black stimuli Ihan for while objecls of Ihe same size, and
(Muntz, 1963b; R. Jaeger and Hailman, 1976; see Chap- loads srrike mainly al Ihe leading objecl when Ihe prey
ter 6). moves orthogonally lo Ihe load's optic axis. Extensive
Depth perception and stereopsis.—Among verte- neurophysiological work on visual sensitivity lo prey stim-
brales two major mechanisms are known for deplh per- uli by Ewert el al. (1978) showed Ihal neurons wilh sen-
ception and stereopsis. One of these, binocular visión, is sitivity lo particular moving configurational stimuli occur
absenl in amphibians Ihat have small, lateral eyes. How- in Ihe retina and retinal projection fields, and Ihal cor-
ever, because of Iheir large, proluberanl eyes, many anu- responding behavior occurs in a class of leclal neurons.
rans and some salamanders have visual fields of nearly However, no neurons are known lo have specific re-
360°. The righf and left fields broadly overlap in some sponses lo a stimulus of only a certain configuration. Also,
anurans, especially centrolenids, and in some plelhodon- inhibilory Ihalamic nelworks play an importanl role in
tid salamanders. Experimente wilh Rana and Bu/o by discrimination belween objecl molion and self-induced
Ingle (1976, and papers ciled therein), Collett (1977), motion. Highly complex inleractions belween visual stim-
and Lock and Collett (1980) demonsfraled Ihal binocular uli and somatic motor coordination are involved in prey
visión (slereopsis) is importan! for depth perception and caplure (see Chapler 9).
accurale movemenls toward prey and avoidance of bar-
riers. Anurans with one ablated eye are less accurale in Extraoptic Photoreception
slriking a prey. Allhough a well-differentialed parietal eye such as known
The olher mechanism is accommodation. This takes in Ihe lualara and in lizards is absenl in amphibians, a
place by a change in the posiüon of Ihe lens wilhin Ihe homologous pineal end organ is presenl in anurans. Ear-
eye. accommodation for near objects is accomplished by lier work on Ihe pineal end organ and ils function was
contraction of the m. prolraclor lentis, which moves Ihe summarized by K. Adler (1970) and Eakin (1973), and
eye toward Ihe cornea. Anurans have lwo protraclor Ihe slruclures were reviewed by Dodl and Meissl (1982).
muscles, whereas salamanders have only one. accom-
modation may be essenlial only in monocular visión, be- Structure. The morphology of the pineal end organ
cause the overall effect of accomodative mechanisms is (= frontal organ or stirnorgan) and associaled neurolog-
small (< 5 diopters); furthermore, Jordán et al. (1980) ical fealures has been described by Oksche (1965), Van
showed Ihat depth estimation in Bufo with suppressed de Kamer (1965), D. E. Kelly (1971), and Ueck el al.
lens accommodation was nearly as precise as thal of nor- (1971). The pineal end organ is presenl in adulto of some
mal toads. G. Roth el al. (1983) suggesled Ihal accom- anurans (e.g., Rana) allhough il is presenl in ladpoles of
modation plays a minor role in deplh perception in many olhers (e.g., Hy/a regula). The end organ appears as a
plelhodontid salamanders, which have an extiremely large nearly pigmenlless spol medially between Ihe anterior
lens proportional to Ihe size of the eye and a short focal edges of Ihe eyes.
length. Moreover, Ihe lenglh of Ihe outer segmente of Ihe The pineal end organ and Ihe pineal body develop
pholoreceplors mighl be sufficienl lo compénsale for var- from a common dorsal pouch of Ihe diencephalon. In
MORPHOLOGY
384 pineal end organ—| — frontoparietal in the pineal body or end organ (Bagnara and Hadley,
epidermis i—melanophores 1970).
dermis Phase shifts of the locomotor rhythm is accomplished
in salamanders (Plethodon glutinosas) with or without
eyes; experiments by K. Adler (1969) strongly implicated
the pineal body as the receptor and regulator for this
circadian rhythm.
Behavioral experiments with many species of anurans
and salamanders have established that (1) orientation
pineal body can be accomplished by celestial cues, (2) the organisms
posterior
commissure must know the local time in order to orient, and (3) eye-
less animáis respond in a manner similar to that of normal
animáis. This compass orientation has been associated
with pineal photoreception and effectively demonstrated
in Acris gryllus (D. Taylor and Ferguson, 1970) and Am-
optic nerve bystoma tigrinum (D. Taylor, 1972). Further experiments
with A. tigrinum (K. Adler and D. Taylor, 1973) revealed
Figure 14-12. Diagrammatic medial sagittal section through the that both normal and eyeless salamanders trained under
brain of Rana temporaria showing the pineal complex and linearly polarized light orient to the bearing of the plañe
associated structures. Adapted from Van de Kamer (1965). (e-vector) of linearly polarized light, but when the top of
the head is covered with opaque plástic orientation is
those anurans with a persisten! end organ, the extra- random.
cranial portion of the pouch is pinched off from the pineal
body and comes to lie in the dermis, whereas the pineal
Olfactory System
body ( = epiphysis) remains in the neurocranium. The
pineal body lies immediately posterior to the paraphysis, Structure. More is known about the anuran olfactory
a secretory pouch on the dorsal wall of the diencephalon system than that of either salamanders or caecilians, but
(Fig. 14-12). The pineal end organ and the pineal body morphologically the organs of the three orders are suf-
are hollow; in salamanders the lumen of the the pineal ficiently similar to suggest that they funcüon in the same
body is obliterated during development. way. The only comparatíve morphological study is Jur-
Both the pineal end organ and the pineal body have gens (1971). A review of the olfactory system by Scalia
receptor cells. The ultrastructure of these cells resembles (1976a) is restricted to anurans.
that of the photoreceptors in the retina of the eye; their Amphibians possess a dual olfactory system—the ol-
outer segments contain a complex of lamellae resembling factory system proper, and the accessory olfactory system
the discs of retinal rods, and the inner segments contain or the vomeronasal organ ( = Jacobson's organ). Each
mitochondria-packed ellipsoids. The pineal end organ is component arises from sepárate receptor organs, follows
innervated by the pineal nerve from the posterior com- parallel but distinct neural channels ¡n the cerebral hemi-
missure of the brain; this nerve apparently is absent in sphere, and probably ¡nvolves different central mecha-
some species (e.g., Hy/a arbórea; Dodt and Heerd, 1962). nisms in the diencephalon. Thus, afferent nerves of the
The pineal nerve contains both afferent and efferent fi- olfactory system proper origínate in the olfactory epithe-
bers. Both the pineal end organ and the pineal body are lium of the nasal organ and termínate upon postsynaptic
sensitive to light intensity and to different wavelengths neurons in the olfactory bulb, whereas afferents of the
(Dodt and Heerd, 1962; Dodt and Jacobson, 1973). accessory system arise from the sensory epithelium of
Jacobson's organ and form the vomeronasal nerve which
Function. The pineal body and in anurans also the terminales in the accessory olfactory bulb.
pineal end organ have been implicated experimentally in The nasal organ lies within, and is supported and pro-
pigmentary adaptation, synchronization of circadian lo- tected by, the rostral part of the skull. If dermal roofing
comotor rhythms, sun-compass orientation, and polar- and palatal bones are well developed (e.g., caecilians).
taxis. internal cartilaginous support of the olfactory organ is
The photoreceptor cells in the pineal body are inhib- minimal. In salamanders and in anurans especially, the
ited by light and sümulated by its absence; stimulation of chondrocranium is elaborated into a complicated frame-
the receptors results ¡n the reléase of melatonin which work that supports the tissues of the principal nasal cavity
contraéis dermal melanophores. Thus, the blanching of (cavum principale), its accessory chambers, and the na-
the skin resulting from melanophore contracüon seems solacrimal duct.
to be controlled by the pineal body, and the stimulus is Basically, the olfactory organ can be thought of as a
the amount of light received by the the photoreceptors system of saclike chambers. The largest of these is the
 Integumentary, Sensory, and Visceral Systems
i principale, which opens anteriorly at the external cipale into a main chamber and lateral diverticulum, of 385
• i -; ;" posteriorly into the buccal cavity at the choana. which the anterior end is specialized by the presence of
-::-:;;:-. chambers are located ventrally and laterally; a well-developed Jacobson's organ.
T-:'-• ' _—bers and positions are variable and will be de- Caeci/ians.—Early descriptions of the nasal organ in-
-:-:--; :r. more detail below. The nasolacrimal duct gen- clude the works of Wiedersheim (1879) and P. Sarasin
í7i_. .; associated with the lateral part of the cavum and F. Sarasin (1887-90). The development of Jacob-
— - : - í.e. although it may open into an accessory cham- son's organ and the tentacular apparatus of /chthyop/iis
:-:- "--.-ir :han into the cavum principale directly. g/utinosus was investigated by Badenhorst (1978), and
T-.€ ciliated epithelium lining the nasal chambers is Jurgens (1971) briefly compared the structure of the cae-
•ganized into two anatomically distinct types—respira- cilian olfactory system with that of salamanders and anu-
«jry and sensory—that are supported in places by glan- rans. A nasal tube leads from the external naris to a long,
nssue. Respiratory epithelium generally is found on depressed nasal sac, the cavum principale. The cavum is
l and lateral surfaces of the cavum principale. The divided into medial and lateral halves throughout the
aaotfle cilia of these cells maintain a continuous flow of posterior two-thirds to three-quarters of its length by the
micous secretion over the entire epithelium. There are olfactory eminence, a longitudinal, ridgelike structure in
tree distinct áreas of sensory epithelium. The most wide- the floor of the cavity. Posterolaterally, the principal
spread occurs on the medial wall, roof, and anterior end chamber is differenüated into two distinct ventral cham-
oí the cavum principale. Nerve fascicles found in the lam- bers—Jacobson's organ and the Choanenschleimbeutel
rs. propria beneath the epithelium converge posteriorly (Fig. 14-13). Jacobson's organ is tubular, and lies nearly
33 give rise to the dorsal división of the olfactory nerve. perpendicular to the long axis of the nasal sac. The glands
7he sensory epithelium covering the elevated portion of of Jacobson's organ are located near the distal end of
the floor of the cavum principale, the eminentia olfac- the structure. The nasolacrimal duct is composed of paired
:rña. is separated from the remaining sensory epithelium tubes which arise from the tentacular sheath, pass through
oí the cavum principale by a perimeter of nonsensory the glands of Jacobson's organ, and unite into a short,
epithelium. Sensory epithelium of the eminential olfac- single tube before terminaüng in the distal end of Jacob-
:oria gives rise to the ventral división of the olfactory son's organ. The Choanenschleimbeutel lies between Ja-
nerve. The third área of sensory epithelium is Jacobson's cobson's organ and the choana and ventral to the lateral
organ which is located in an accessory chamber to the part of the cavum principale. The Choanenschleimbeutel
cavum principale. This epithelium gives rise to the vo- is not connected to Jacobson's organ; instead, it com-
meronasal nerve. municates by means of a so-called communal cavity with
The cilia of the sensory epithelia presumably are sen- the lateral part of the cavum principale. The epithelial
sitivo to chemical materials that are in solution in the lining of these structures corresponds to that of the cavum
mucous covering of the nasal epithelium, but little is known principale and is composed of simple, ciliated columnar
about actual olfactory behavior or function. cells interspersed with numerous goblet cells.
Salamanders.—Of the three orders of amphibians, the The tentacular apparatus lies lateral to the nasal sac
olfactory system is simples! in salamanders (Jurgens, 1971, with its posterior end directed dorsally and its anterior
and references cited therein). The organ consists primar- end directed ventrally. The apparatus consists of the ten-
ily of a large chamber (cavum principale) that lies be- tacular sheath and tentacle anteriorly and a retractor muscle
rween the external naris and the choana. The cavum posteriorly. The sheath extends posteriorly from the ex-
principale has a ventrolateral extensión (Fig. 14-13) known ternal orífice to the orbit where it endoses the orbital or
as the lateral diverticulum that extends beyond the level Harderian glands that fill the orbit. The tentacle is formed
of the choana as a fold, the sulcus maxillo-palaünus. The from the wall of the sheath, and consists of an inner mass
lateral diverticulum can be subdivided into anterolateral of connective tissue that is surrounded by an epithelial
and posterolateral parís. The nasolacrimal duct runs from layer. The distal end of the tentacle is free; thus, it can
the eye to the anterolateral portion of the lateral diver- be moved in and out of the sheath by the retractor mus-
ticulum where it opens in the área of sensory epithelium cle that arises from the lateral wall of the neurocranium.
of Jacobson's organ. The posterolateral portion of the This muscle is homologous with the m. levator bulbi of
lateral diverticulum that communicates with the buccal salamanders and anurans and is innervated by C.N. VI
cavity lacks sensory epithelium. There is considerable (abducens). According to Jurgens (1971), the tentacle is
variation in the complexity of the olfactory organ among lubricated by secretions from the Harderian glands as it
salamanders. It is the least complex in aquatic taxa, and moves in and out of the tentacular sheath. Chemical sub-
tends to be more complex in more terrestrial species. stances are transported from the tentacle via the sheath
Thus, Amphiuma and Siren lack a nasolacrimal duct, and to the nasolacrimal ducts and thence to Jacobson's or-
in Amphiuma, the proteids, and Cryptobranchus, Jacob- gan. Thus, when caecilians are burrowing and their nos-
son's organ is reduced. In contras!, terrestrial species are trils presumably are closed, they are capable of chemo-
characterized by greater differentiation of the cavum prin- sensory perception. Air routed through the nostrils probably
MORPHOLOGY
386 B
ext naris
ext naris

c med -f/
c inf (lat rec)-|V/
íL
f to*
c inf (lat rec) nasolac d- olf n
nasolac d -1—olf n
I c prin /

c inf
(Jo)

Figure 14-13. Schematic drawings

of amphibian nasal organs. A. The
salamander Trituras alpestris in
dorsal view. B. The anuran Ascaphus
truel in dorsal view. C. The
salamander Ambystoma maculatura
in lateral view. D. Ascaphus truel in
lateral view. E. The caecilian ext
íchthyophis glutinosas in lateral naris
view. F. Ambystoma maculatura in
ventral view. G. Ascaphus truel in
ventral view. H. íchthyophis
glutiaosus in ventral view.
Abbreviations: c med = cavum
médium, c inf (lat rec) = cavum
inferius (lateral recess), c. prin =
cavum principale, Chb =
Choanenschleimbeutel, ext naris =
externa! naris. Jo = Jacobson's
organ, naslac d = nasolacrimal duct,
olf n = olfactory nerve, S maxpal =
sulcus maxillopalatinus, tr =
tentacular refractor muscle, ts =
tentacular sheath. All redrawn from
Jurgens (1971).

is shunted directly through the cavum principale and into lateral portions. The medial part (diverticulum medíale of
the buccal cavity through the choana via the common the cavum inferius) represents Jacobson's organ, whereas
chamber and the Choanenschleimbeutel. the lateral part (diverticulum laterale of the cavum infer-
Anurans.—The structure of the nasal organ in anurans ius) lacks olfactory epithelium and opens into the choana
was investígated by Helling (1938), and summarized by and buccal cavity. The diverticulum laterale is assumed
Jurgens (1971; see included references). In contrast to to be homologous with the sulcus maxillo-palatínus of
salamanders, the organ is differentiated into three distínct salamanders. The cava inferius and principale are joined
chambers (Fig. 14-13). The largest, the cavum principale, anterolaterally by a small chamber, the cavum médium,
extends from the level of the external naris to the choana. which lacks olfactory epithelium. The nasolacrimal duct
The diverticulum laterale is differenüated as the cavum extends from the eye to open into the cavum médium.
inferius in anurans, and is subdivided into medial and In primitive anurans (e.g., leiopelmatids and discoglos-
 Integumentary, Sensory, and Visceral Systems
sids), the cavum médium and the eminentia olfactoria panic membrane), which receives airborne vibrations. 387
nd to be smaller than in advanced anurans. All anurans These are directed toward the tympanum by fleshy re-
possess a nasolacrimal duct. flectors in mammals. Most anurans have a distinct tym-
panic membrane, a thin layer of integument stretched
Function. The olfactory receptors functíon in che- over a carülaginous annulus in a drumlike manner. In
moreception (see review by Madison, 1977). The cae- some anurans the tympanic annulus is absent. In such
rilian tentacle probably is the primary receptor used in aurans and in salamanders and caecilians there is no
kxating food and also may play a role in locatíng mates. differentiated tympanum.
Numerous studies have shown that anurans use olfactory A middle ear, or tympanic cavity, ¡s present only in
cues for orientatíon, especially to familiar breeding sites anurans. The columella ( = stapes), which is homologous
see Chapter 3) and to recognize the odor of particular to the hyomandibular of fishes, transmits vibrations from
prey (Martof, 1962b; Kmelevskaya and Duelina, 1971; the tympanic membrane to the membrane covering the
Gesteland, 1976; K. Müller and Kiepenheuer, 1976). oval window ( = fenestra ovalis or fenestra vesübuli), which
Olfactory communicaüon is well developed among sepárales the middle ear from the inner ear. The colu-
plethodontid salamanders, which have a nasolabial groove mella has an expanded proximal end, or footplate, against
leading from the margin of the upper lip (commonly in- the membrane of the oval window, a space that is shared
duded in an elongate cirrus) to the nares (C. Brown, by the operculum, part of the system for transmitting
1968). These salamanders are capable of picking up ol- substrate vibrations to the inner ear. The columella is
factory cues from the substrate. Experimental studies on reduced or absent in some anurans that lack a tym-
various species of P/ethodon have shown that these sal- panum. A canal (Eustachian tube) connects the middle
amanders can identífy conspecifics as well as individuáis ear with the pharynx in anurans; airflow in the Eustachian
of other species (see R. Jaeger and Gergits, 1979, for tube equalizes pressure on either side of the tympanic
review). membrane. The middle ear and Eustachian tube are ab-
sent in salamanders and caecilians. In the latter the col-
Auditory System umella articulates with the quadrate; proximally it is fused
Amphibians have evolved an auditory apparatus that is with the operculum, or an operculum is absent. In sala-
unique among vertebrales; it contains a combinaüon of manders the columella articulates distally with the squa-
structures that function in the transmission of substrate mosal in larvae, and its articulatíons are variable in adults
vibrations and, especially in anurans, airborne sound (see Chapter 13).
waves. The ears of salamanders have been studied by The inner ear, or membranous labyrinth, is suspended
Monath (1965) and Lombard (1977), and those of cae- within the otic capsule by loóse connective tíssue. The
cilians by Wever (1975) and Wever and Gans (1976). labyrinth consists of a perilymphatic (= periotic) fluid
Anurans vocalize, and their ears have been the subject system and an endolymphatic fluid system, each con-
of many kinds of investígations (see Chapter 4); the prin- tained within distinct sets of membranes (Fig. 14-14). The
cipal morphological studies have been by Wever (1973, perilymphatíc system consists of a large cistern against
1979) and E. Lewis (1984). which the operculum and footplate of the columella rest
in the oval window. The perilymphatic system is con-
Structure. Generally the tetrapod ear consists of three nected by a duct to the perilymphatic sac which lies in
parts. The outer ear consists of the tympanum (or tym- the neurocranium. Branches of the perilymphatíc duct

perilymphatic d otic capsule

utriculus
papilla amphibiorum
endolymphatic sac ant semicircular d
póst semicircular d
horiz semicircular d
columella
medulla
oblongata tympanum
operculum
ganglion
perilymphatic d Figure 14-14. Schematic diagram of the ear of
the bullfrog. Rana catesbeiana; posterior view of
round window- right ear. Bone and cartilage are hatched; the
oval window perilymphatic system is coarsely shaded, and
papilla basilaris—' '—lagena ^perilymphatic the endolymphatic system is finely shaded.
cistern Adapted from Frishkopf and Goldstein (1963).
MORPHOLOGY
388 a but the chambers of the papilla amphibiorum and pa- tact membrane against the perilymphatic fluid. The size
pilla basilaris of the sacculus of the endolymphatic sys- and arrangement of the papilla amphibiorum are highly
tem. variable, as are the number and polarization of the hair
The endolymphatic system consists of the receptor or- cells. In advanced anurans, such as Rana catesbeiana,
gans of the inner ear. The basic structure of the endo- there are about 600 hair cells, each containing 70-80
lymphatic system consists of two large vesicles, the dorsal stereocilia and one kinocilium. The tips of the cilia ap-
utriculus and the ventral sacculus. The lagena is a pouch proach a gelatinous tectorial membrane that is suspended
off the posteroventral surface of the sacculus. Two other from the sensory surface of the chamber and covers the
small pouches off the sacculus are the dorsal chamber of full extent of the papilla. The cells do not sit on a basilar
the papilla amphibiorum and the ventral chamber of the membrane; instead, they are imbedded in the labyrinth
papilla basilaris. Two vertical semicircular ducts (cañáis) wall. The amphibian papilla receives both afferent and
diverge from the terminus of a dorsal extensión of the efferent nerve fibers. The general topography of the sen-
utriculus, the cruz commune, and the horizontal semicir- sory surface consists of a single patch of hair cells in
cular duct diverges from its base. All three ducts enter caecilians and salamanders. In most anurans the sensory
the utriculus via ampullae containing receptor cells. surface seems to consist of two contiguous patches, the
An endolymphatic duct leads from the sacculus to the more posterior of which is conspicuously elongated and
endolymphatic sac in the neurocranium. This sac is small curved. E. Lewis (1984) demonstrated that there is a
in most salamanders, but the sacs are expended in some grade in elongation and complexity of the surface of the
salamandrids, and those on either side coalesce dorsal to neuroepithelium and that this grade corresponds to the
the brain in Ambystoma. In anurans, the endolymphatic general scheme of anuran phylogeny.
sacs are fused and consist of a ring around the brain, a E. Lewis (1981, 1984) summarized the morphological
posterior extensión into the vertebral canal, and in many features distinguishing the papilla amphibiorum of sala-
species an anterior intercerebral porüon (Dempster, 1930). manders and that of anurans. The typical anuran struc-
The neuroepithelium of the inner ear is located in well- ture consists of two patches of neuroepithelium, each
defined áreas, and these receptors are innervated by innervated by a sepárate branchlet of the auditory nerve
branchlets of the posterior branch of the auditory nerve and each having two populations of oppositely polarized
(C.N. VIII). Neuroepithelial cells are like neuromast cells. hair cells; the salamander structure consists of a single
Each cell has many stereocilia and one kinocilium. The patch innervated by one branchlet of the auditory nerve
neuroepithelial cells in the ampullae (cristae ampullae) of with a single pair of populations of oppositely polarized
the semicircular ducts have their cilia imbedded in a ge- hair cells. In anurans the perilymphatic duct is in contact
latínous membrane, or cúpula, as do the cells in a sensory with the posterior end of the amphibian chamber, whereas
patch in the utriculus called the crista neglecta (in am- in salamanders the duct is in contact with the medial
phibians, present only in caecilians). Other patches in the surface of the chamber. The tectorial membrane is thick
neuroepithelium in the utriculus, sacculus, and lagena are where it is adjacent to the anterior patch of neuroepi-
referred to as maculae; structurally these cells are like thelium and thin adjacent to the posterior elongation in
those in the cristae, except that inorganic crystals (oto- anurans; in salamanders it is of a uniform intermedíate
liths) are present in the cúpula. thickness over the entire papilla. The kinocilia in anurans
The papilla basilaris and papilla amphibiorum are termínate in a bulb, whereas the kinocilia in salamanders
patches of neuroepithelium contained in sepárate pouches; lack a bulb. Limited observations on caecilians indícate
the papilla amphibiorum is unique to amphibians. that the structure of the papilla amphibiorum is like that
The basilar chamber contains hair cells arranged cir- in salamanders.
cumferentíally around the lumen of the chamber that The results of E. Lewis's (1981, 1984) ultrastructural
opens directly into the sacculus on one end and on the studies have phylogenetic significance. Leiopelmatíd frogs
other terminates in a thin contact membrane separating are like salamanders in having a single patch of neuro-
it from the perilymphatic system. The cells sit on a basilar epithelium with a single pair of populations of oppositely
membrane. Each hair cell has numerous stereocilia and polarized hair cells (Fig. 14-15), the perilymphatic duct
one kinocilium; all are oriented with the kinocilium to- being in contact with the median surface of the chamber.
ward the contact membrane. The cilia are attached to an the tectorial membrane being of uniform thickness, and
overlying gelatinous tectorial membrane which parüally the kinocilia lacking terminal bulbs. In anurans, other than
filis the cross section of the chamber. The papilla basilaris leiopelmatids, the kinocilia of the hair cells in the lagena.
is innervated only by afferent nerve fibers. The papilla sacculus, and papilla basilaris also have terminal bulbs
basilaris is present in all three living orders of amphibians, (E. Lewis, 1981). The development of kinociliary bulbs
but it is reduced in size in some salamanders and absent is an ontogenetic phenomenon in Rana catesbeiana
in all sirenids, proteids, and plethodontids, and in some (E. Lewis and Li, 1973). Also, the confluence of the an-
salamandrids (Lombard, 1977). terior and posterior patches of neuroepithelium seems to
The amphibian chamber also terminates in a thin con- be an ontogenetic phenomenon; in Xenopus laeuis and
 Integumentary, Sensory, and Visceral Systems
• :¿tesbeiana, the two patches are not contiguous in over the papillae basilaris and amphibiorum. From the 389
srv larval stages but gradually merge in later larval stages latter, a membranous window leads to the perilymphatic
L: and E. Lewis, 1974). duct and on to the perilymphatic sac within the neuro-
cranium. Thereafter, the pathway traverses the arachnoid
Function. The neurophysiology of the inner ear, espe- membrane to the cerebrospinal fluid and extends across
óafiy that of anurans, has been the subject of intensivo the midline, mainly beneath the brain, and continúes
sruáy. The inner ear functions to maintain equilibrium through a reverse order through the same structures to
2T.c to transmit vibrations from the air or substrate to the the contralateral oval window. Thus, ¡n salamanders re-
btain. The receptor organs in the inner ear are charac- ception invariably is binaural.
Krized by innervated epithelial surfaces studded with Auditory reception.—The sensory receptors in the in-
ser.sory receptor cells and an acellular mechanical net- ner ear of all amphibians are sensitive to seismic (sub-
•ork consisting of both fluid and solid elements. Electro- strate) vibrations, and those in anurans are sensitive to a
-r.ysiological evidence indicates that the stereocilia of the wide range of airborne frequencies. Electrophysiological
receptor cells are sensitive to strain and that the acellular studies on salamanders by Ross and J. Smith (1980)
T.echanical network serves as part or all of a filter that revealed that receptors in the sacculus are sensitive to
>e]ects particular mechanical sümuli, transíales them into frequencies of 20 to 450 hertz (Hz) and that sensitivity
rsreociliary strain, and rejects other mechanical stimuli. seems to be related to the habitat. For example, peak
Ir. this way, the acellular networks are partly or totally sensitivity in terrestrial efts of Notophthalmus uirídescens
responsible for the efficient stimulus selectívity of the in- is 150-250 Hz, whereas that of aquatic adults is 150 Hz.
r.¿r ear. Terrestrial Plethodon cinerus have a peak sensitivity of
The stereocilia are immersed in the endolymphatic fluid, 200-250 Hz, but larvae of Ambysíoma macu/aíum have
2T.d the stimulation of these receptor cells is by means a peak of only 200 Hz. Wever and Gans (1976) reported
D: mobilization of the perilymphatic and endolymphatic a peak sensitivity of 200 Hz in the caecilian Ichthyophis
ñuids. The perilymphatic fluid is mobilized by vibrations glutinosas.
D: the operculum or the footplate of the columella against A high degree of sensitivity to seismic vibrations has
±e membrane at the oval window. These vibrations may been reported in anurans. Receptors in the sacculus and
origínate from the substrate and are transmitted via tonic lagena of Rana caíesbeiana are sensitive to frequencies
responses of the opercularis muscle extending between of 15-200 Hz (Koyama et al., 1982); low frequencies
the pectoral girdle and the operculum. In most anurans, (20-160 Hz) produced by Leptodactylus albilabris and
airborne sound waves are transmitted via the tympanum transmitted by the substrate are selectively received by
and columella to the oval window. Sensitivity to airborne the sacculus in other individuáis (E. Lewis and Narins,
sounds is maximized by the large size of the tympanum 1985).
compared with the size of the oval window; in this way Airborne sound waves are transmitted via the tym-
the acoustic impedance of the air is matched with the panum and columella to the inner ear, where mobiliza-
higher impedance of the fluids in the inner ear (Capran- tion of the perilymph is coupled with the endolymph to
ica, 1976). Oscillation of the perilymph is transmitted to créate motion of the tectorial membranes and stereoci-
the endolymph via common membranes. liary strain on the receptor cells of the papilla amphi-
The displacement of fluids in the inner ear occurs in biorum and papilla basilaris. The receptors of these au-
different ways in anurans, caecilians, and salamanders ditory epithelia are sensitive to different frequencies.
(Wever, 1978). Anurans have a round window in the Electrophysiological evidence (Capranica, 1965; Chung
otic capsule which is bounded by the perilymphatic et al., 1978; Koyama et al., 1982) shows that the greatest
membrane. Vibratory sound pressures exerted against sensitivity of the receptors in the sacculus is 20-150 Hz
the oval window oscillate the perilymph between the oval in most anurans. Henee, these receptors have a low sen-
window and the round window; the inward displacement sitivity to airborne sounds but a high sensitivity to seismic
at the oval window is accompanied by an outward dis- vibrations. The greatest sensitivity of the papilla amphi-
placement of equal volume at the round window. Cae- biorum is from 100 to 1000 Hz and that of the papilla
cilians and salamanders lack a round window. In caeci- basilaris is from 1000 to 5000 Hz. The presence of both
lians, vibrations against the oval window set the perilymph kinds of papillae, the impedance-matching system of the
in motion along a roundabout course back to the oval middle ear, and the interlocking columellar-opercular
window; the fluid surges back and forth along this path- mechanism provides anurans with an efficient mecha-
way. In salamanders, pressure exerted against the oval nism for acoustic reception (see Chapter 4).
window produces fluid displacements that traverse a Selection of frequencies in anurans also is accom-
complex path across the head to the contralateral oval plished by tonotopic organization of the sensory patches
window. The pathway leads through three different fluids of the papilla amphibiorum (E. Lewis, 1981; E. Lewis et
beginning with that in the perilymphatic cistern and then al., 1982). Frequencies are sorted by a combination of
to the endolymph in the sacculus, where the motion passes two patches of neuroepithelium with sepárate innerva-
MORPHOLOGY
390

Figure 14-15. Scanning electrón micrographs

of neuroepithelial surface of the papilla
amphibiorum in the inner ear; the sensory
surface is identified by the presence of projecting
hairlike tufts. A. Ascaphus truel. B. Pipa pipa.
C. Pelobates fuscus. D. Knssina senegalensis.
Photos courtesy of E. R. Lewis.

tions, a tectorial mcmbrane with spatially graded bulk, of the hair cells. Apparently the crista neglecta in caeci-
the position of the contact membrane at the posterior lians also is a receptor for head motions (Wever and
end of the chamber instead of along its medial margin, Gans, 1976).
and possibly by the polarization of the hair cells. In anu-
rans, such asAscap/ius truei (Fig. 14-15A), and presum-
ably in salamanders and caecilians with a single patch of NERVOUS SYSTEM
papilla amphibiorum, the frequency range of sensitivity Although the nervous system of amphibians is somewhat
is 100-600 Hz. Extensión of this frequency range beyond more highly developed than that ¡n fishes, amphibians
600 Hz seems to depend on the posterior elongation of retain the primitive pattern of nerve-cell bodies around
the posterior patch of hair cells. This was shown to be the venírteles of the brain. In contras! to the everted fore-
the case in the elongate patch in Rana catesbeiana by brain of fishes, there is an invagination of the hemi-
E. Lewis et al. (1982), who determined the best excita- spheres in amphibians; this construction is like that of
tory freqencies for auditory stimuli of 29 afferent axons amniotes, which, unlike amphibians, have a definitive
of the auditory nerve innervaüng the papilla amphibiorum. cerebral cortex. Amphibians have two meninges, a vas-
Fourteen axons with frequencies at or below 300 Hz cularized pia mater attached to the brain and spinal cord
terminated in the anterior región of the papilla; ten axons and a tough, outer dura mater adjacent to the bones.
with frequencies of 400-550 Hz terminated in the central Herein the classic regions of the nervous system are
región; and five axons with frequencies of more than discussed in the following order—brain, cranial nerves,
550 Hz terminated in the posteriormost región. spinal cord and spinal nerves, and autonomic nervous
Equilibrium.—The neuroepithelia and associated ge- system. Some developmental aspects of the nervous sys-
latinous cupulae of the crista ampullae and the maculae tem are discussed in Chapter 7. Neurophysiology and
of the utriculus, sacculus, and lagena are equilibrium re- ultrastructure are treated only in a general way; an ex-
ceptors. According to the summary by E. Lewis and Lev- tensive literature is available on these subjects (see
erentz (1983), in the semicircular ducts the viscosity and J0rgensen, 1974; Llinás and Precht, 1976; and Oksche
inertia of the endolymph apparently combine with the and Ueck, 1976).
viscoelasücity of the cupulae to transíate rotational mo-
tions about particular axes into stereociliary strain; at the Brain
same time, rotational motion about the orthogonal axes The morphology of the brain has been studied in ñaña
and linear motion along any axis are rejected. The cal- escalenta by Gaupp (1896); nearly all modern treatments
cariferous masses of the otolithic maculae and the vis- of the gross morphology of the anuran brain are based
coelastic gelatinous membrane associated with each sen- on that work. Kuhlenbeck (1922) provided a detailed
sory patch apparently combine to transíate linear motion description of the brain of the caecilian Hypogeophis ros-
into stereociliary strain. Directional selectivity in the mac- tratas, and Kuhlenbeck et al. (1966) presented additional
ulae appears to be provided by the polarization patterns information on the forebrain of caecilians. The brain of
 Integumentary, Sensory, and Visceral Systems
Siomandra sa/amandra was described by Francis (1934), nerve is comparatively massive. Each cerebral hemi- 391
and the most exhaustive study is that by Herrick (1948) sphere is divided into a dorsal pallium and ventral sub-
-•-. Ambysíoma tigrinum. Noble (1931b) made general pallium; their distinction is marked by a sulcus on the
romparisons of the brains of the three living orders of inner surface of the ventricles and in anurans by a groove
2—phibians. on the outer surface. In the subpallium, a medial septum
is distinguished from lateral basal ganglia. Also, the pal-
Forcbrain. The forebrain is differentiated into the tel- lium is differentiated into an internal hippocampus and
sr.cephalon and diencephalon (Fig. 14-16). The telen- external pyriform primordium.
rephalon is composed of a pair of bilateral olfactory bulbs Differentiation of an accessory olfactory lobe in the
and cerebral hemispheres; it is shorter but farther invag- anterior part of the cerebral hemisphere occurs in cae-
ir.ated in anurans than in salamanders and caecilians. cilians and anurans; it is poorly developed in most sala-
The olfactory nerve (C.N. I) exits from the anteroventral manders and is absent in oblígate neotenes. The degree
surface of the olfactory bulb in anurans and hynobiid of development of the accessory olfactory lobe is posi-
salamanders and from the anterolateral surface in other tively correlated with development of Jacobson's organ,
salamanders and caecilians; in the latter, the base of the which is absent in neotenic salamanders. The amygdaloid

habenular gang—| —pineal organ

choroid plexus optic lobe
cerebral hemisphere

pituitary

optic chiasma infundibulum

cerebral hemisphere

Gasserian gang ventral cerebral

artery
r opthalmicus
profundus

pineal organ ,,,,-T - optic chiasma

r maxillaris
thalamus :;^-ü hypothalamus

optic lobe IV
r mandibularis pituitary
Vil cerebellum

acoustico- medulla oblongata IX &X

facialis gang
glossopharyngeal
vagus gang basilaris artery

Figure 14-16. Brain of Salamandra salamandra. A. Lateral (midsagittal section). B. Dorsal. C. Ventral.
Cranial nerves are indicated by román numeráis. Abbreviations: gang = ganglion, r = ramus. Adapted from
Francis (1934).
MORPHOLOGY
392 nucleus (a prominence on the lower surface of the cere- important center for control of the autonomous nervous
bral hemisphere) ¡s correspondingly well developed in system.
anurans and caecilians, as is the striatum (external tissue
of the subpallium). The relative development of the latter Midbrain. The midbrain, or mesencephalon, is made
also seems to be correlated with an increase ¡n extero- up of the dorsal tecta (optic lobes) and the basal teg-
receptive tracts. mental or peduncular portion. The latter transmits motor
The telencephalon is the receptor for sensory impulses impulses. The peduncular región receives fibers from
derived from the olfactory epithelium of the nasal sacs practically all parts of the brain anterior to the medulla:
and from Jacobson's organ. Although there is a concen- its primary function is to control mass movements of the
tration of olfactory fibers in the olfactory bulbs (and ac- body and limbs. Also, this is the site of origin of two eye
cessory olfactory lobes when present), all parís of the muscles (C.Nn. III and IV).
cerebral hemispheres receive impulses from the olfactory The optic lobes and tissues composing the optic tectum
fibers. The septum and striatum are synaptíc stations where are best developed in anurans and least developed in
olfactory fibers join with fibers from the thalamus and caecilians. In anurans, the tectum has white and gray
midbrain. A peripheral wandering of cells from the hip- strata. Fibers from the optic tract spread throughout the
pocampus and pyriform áreas ¡s most extensive in anu- tectum. The function of the optic tectum is the visual
rans. In amniotes, these cells lead to the development of control over movements of the body as a whole, and
cell laminae in the pallium sepárate from the periventri- particularly the orientation of the body and conjúgate
cular cells; these laminae cells differentiate into correla- movements of the eyeballs with reference to objects in
tion centers, whereas the periventricular cells remain the visual field.
pathways for relatively simple reflexes. Just below the optic lobes is the torus semicircularis.
The unpaired posterior part of the forebrain, the dien- This subtectal cluster of cells is the principal receptor site
cephalon, consists of three major parts—epithalamus, for afferent auditory fibers from the bulbotectal tract in
thalamus, and hypothalamus. The epithalamus is com- the cerebellum.
posed of the habenular ganglia, a choroid plexus (a vas-
cularized invagination ¡nto the third ventricle), and the Hindbrain. The posterior part of the brain consists of
pineal organ. The habenular ganglia receive fibers from the cerebellum and the medulla oblongata (rhomboen-
the telencephalon. A tract of olfactory fibers, the fasci- cephalon), which is continuous with the spinal cord. The
culus retroflexus, extends posteroventrally from the ha- cerebellum consists of paramedian dorsal protrusions and
benular ganglia to the interpeduncular nucleus in the a more lateral pair of auricular lobes that are an anterior
mesencephalic tectum; in salamanders, this nucleus continuation of the acousticolateralis system of the me-
projects posteriorly into the medullary tectum, but this dulla. The histológica! structure of the cerebellum of anu-
projection has not been noted in anurans or caecilians. rans is more complex than that of other amphibians.
The pineal organ (= epiphysis) is a small projection, Anurans have a cerebellar nucleus and tracts to the pe-
best developed in anurans, attached to the dorsomedian duncular región of the midbrain. Also, in anurans there
surface of the epithalamus by a few fibers. These fibers is true lamination of cells and fibers, and the Purkinje
contain the frontal and pineal tracts (parietal nerve), fi- cells (interlaminar flask-shaped cells) have a more defin-
bers of which enter the pretectal región in the posterior itive structure than in other amphibians.
part of the epithalamus. The lateral and ventral walls of In comparison with other vertebrates, the cerebellum
the diencephalon are constítuted by the thalamus, which is small, especially in terrestrial adult amphibians. It is the
contains a web of connecting fibers with all contiguous center for motor coordination, and the small size presum-
parts of the brain, which make the thalamus an importan! ably is correlated with the comparatively simple loco-
center for sensory correlatíon. For example, even though motor activities of amphibians. The degree of develop-
the optic nerves enter the neurocranium and have a ment of the auricular lobes is correlated with the presence
chiasma under the thalamus, these optic tracts pass pos- of a lateral-line system. Thus, larvae and neotenic sala-
terodorsally to the optic lobes of the midbrain. However, manders have proportionately larger auricular lobes.
on their way to the midbrain the optic tracts give off Situated between the cerebellum and the medulla is
collateral fibers which synapse in the thalamus with fibers the isthmus, a región which is distinct in early develop-
of other sensory systems. ment, but which becomes incorporated into the anterior
Posteroventrally, the hypothalamus is a bilobate pro- part of the medulla in adults. Afferent fibers coming from
jection of the diencephalon. The hypothalamus is divided practically all parts of the brain termínate in the isthmus.
into preoptic and tuberoinfundibular regions. In addition Here, too, is the chief sensory nucleus of the trigeminal
to numerous connecting fibers with the ventral thalamus, nerve (C.N. V). Efferent fibers from many centers con-
the magnocellular preoptic nucleus is connected with the verge in the isthmic tegmentum. The isthmic región is the
ventral lobe of the hypophysis, and distinct áreas of the chief regulator of the jaw musculature.
parvocellular tuberoinfundibular nuclei are connected with The medulla is the widened and flattened anterior part
the hypophysial portal vessels. The hypothalamus is an of the spinal cord, from which it differs by having a largely
 Integumentary, Sensory, and Visceral Systems
T.embranous dorsal surface with a cluster of blood ves- review of anurans, Nieuwenhuys and Opdam (1976:813) 393
tís, which forms as the choroid plexus a vascular diver- stated: "In this survey we have relied heavily on the ex-
rculum extending into the ventricle of the medulla. Like haustive analysis of Gaupp (1896)." Gaupp's work was
~e spinal cord, the medulla ¡s divided into a ventrome- on one species of anuran, Rana escalenta. Basic descrip-
¿an motor región and a dorsolateral sensory región. The tive morphology of the cranial nerves of salamanders was
!a:er is the acousticolateralis región, which merges with done by Coghill (1902) on Ambystoma tigrinum and by
dic auricular lobes of the cerebellum. Between the dorsal H. Norris (1908, 1913) and by Francis (1934) on Am-
and ventral portions of the medulla is a región of synaptic phiuma means, Siren lacertina, and Salamandra sala-
runction of sensory and motor fibers. In the anterior part mandra, respectively. The work of earlier authors is re-
:: this región in salamanders are the giant Mauthner cells viewed by H. Norris and Hughes (1918) in their description
which have axons that extend the length of the spinal of the nerves in a few species of caecilians.
cord to the caudal musculature; these fibers function in In the following synopsis, which is based entirely on
r-.e regulation of swimming movements. Vestibular and the literature concerning a few species, the cranial nerves
in larvae) lateral-line fibers have synapses with Mauthner (C.N.) are described; unless specified otherwise, the de-
cells. scription is applicable to all three living orders.
In primitive tetrapods, more of the medulla was con-
•ained within the skull than in living amphibians, so that C.N. I (Olfactory). The first visceral sensory nerve
all 12 cranial nerves exited from the skull. In living am- leaves from the ventrolateral border of the olfactory lobe
phibians, the hypoglossus nerve (C.N. XII) is associated and passes through the fenestra olfactoria into the nasal
.«.ith the first spinal nerve. Of the 11 cranial nerves exiting capsule where it divides into the ramus profundus and
from the skull, 7 (C.Nn. V-XI) enter the medulla and the ramus dorsalis. Fibers of the ramus dorsalis enter the
send afferent and efferent fibers to specific locations within olfactory lobe proper and are connected via olfactory
the medulla. In the ventral motor portion of the medulla, tracts with secondary olfactory centers in the cerebral
the nuclei of the cranial nerve fibers are arranged in nu- hemisphere. The fibers of the ramus profundus extend
merical order; this separation (particularly nuclei of C.Nn. posteriorly into the accessory olfactory bulbs. The ramus
VII. IX, and X) is more evident in anurans than in other dorsalis innervates the olfactory epithelium of the nasal
amphibians. The sensory nuclei of C.Nn. V and VII are sac. The main branch of the ramus profundus innervates
anastomosed in salamanders but not in anurans. the vomeronasal epithelium of Jacobson's organ, and the
The medulla controls actions of swallowing, digestión, ramus medialis nasi pierces the roof of the nasal capsule
heartbeat, and respiration, as well as jaw action and some to supply the skin of the dorsal snout. Various other
locomotor responsos. branches of the ramus profundus seem to be homolo-
Fibers of the auditory nerve (C.N. VIII) enter the me- gous in the living orders, although different ñames have
dulla as discrete branches through a dorsal root and a been used (Jurgens, 1971). The principal variations in
ventral root, where they become associated with a dorsal these are: (1) the branches in Xenopus are similar to
medullary nucleus of small cells and a ventral nucleus of those of salamanders (Paterson, 1939), (2) Cryptobran-
large cells, respectively. Anurans are unique among an- chus is different from other salamanders in that the ramus
amniotes in having a pair of superior olivary nuclei, lo- lateralis nasi does not enter the nasal capsule secondarily,
cated on the ventral side of the medulla. Cells of the and (3) in caecilians the ramus lateralis nasi innervates
superior olivary nucleus receive input from the dorsal the tentacular sheath, and the ramus medialis nasi is di-
medullary nucleus and the contralateral superior olivary vided into two main branches.
nucleus. Fibers from the dorsal medullary and superior
olivary nuclei form the lateral bulbotectal tract which ex- C.N. II (Opticus). This somatic sensory element ac-
tends anteriorly to the torus semicircularis of the mid- tually is part of the brain. It enters the floor of the dien-
brain. Anurans also have a large nuclear mass, the nu- cephalon where it crosses with its contralateral counter-
cleus isthmi, in the tegmentum; it may have some auditory part to form the optic chiasma. After crossing, the nerve
function. The function of the complex auditory receptor ascends the lateral wall of the diencephalon as an exter-
system in anurans is discussed in Chapter 4. nal bundle of fibers, the tractus opticus. Most of these
Finally, the medulla exits the cranium through the for- fibers spread in the superficial layer of the roof of the
amen magnum and becomes the spinal cord. Although midbrain, but smaller contingents termínate in the thal-
there are nerve fibers from the medulla anteriorly into amus, hypothalamus, and tegmentum of the midbrain.
the midbrain and fibers from the forebrain posteriorly into The optic nerve exits the neurocranium via the large optic
the midbrain, there is no uninterrupted pathway from the foramen (or fenestra), which is an hiatus between the
forebrain to the spinal cord. sphenethmoid and prootic. The nerve is covered by a
fibrous connective-tissue sheath and is continuous with
Cranial Nerves the layer of nerve cells on the inner surface of the eye.
The cranial nerves of amphibians have received only cur- In caecilians in which the eye is covered by skin (e.g.,
sory attention for more than 50 years. In the most recent Dermophis, Geotrypes, /chthyophis), the optic nerve is
MORPHOLOGY
394 rudimentary; it passes from the optic foramen, along the A ventral branch anastomoses with the ramus palatinus
retractor muscle of the tentacle, and through the orbital (C.N. VII) and innervates the tissues of the mouth under
glands to the eye. In caecilians in which the eye is vestigial the nasal organs; this anastomosis is absent in caecilians.
and covered by bone (e.g., Caecilia, Oscaecilia), the optic Shortly after leaving the Gasserian ganglion, the ramus
nerve is absent. The optic nerve is greatly reduced in maxillo-mandibularis, which contains both visceral motor
diameter in subterranean salamanders; the nerve is con- fibers and somatic sensory fibers, bifurcates. The ramus
tinuous with the brain in Proteus and Haideotríton but maxillaris has three major branches; two of these supply
usually not in Typfi/oíriton (Brandon, 1968). the skin of the eyelids and the temporal región of the
head, whereas motor fibers innervate the eye muscle.
C.N. III (Oculomotorius). The fibers of the third nerve m. levator bulbi (except in caecilians, all of which lack
emerge from the ventral surface of the mesencephalon this muscle). The ramus mandibularis also contains so-
and exit the neurocranium via the oculomotor foramen matic sensory and visceral motor fibers; it divides into
just posterior to the optic foramen. The bulk of the nerve three major branches. One of these supplies the m. lev-
consists of somatic efferent fibers that innervate four eye ator mandibulae, and another innervates the skin over
muscles. Within the orbit the nerve divides into two rami; the angle of the jaw and the posterior mandible. The
the ramus superior innervates the m. rectus superior, and primary mandibular branch divides into a ramus men-
the ramus inferior innervates the m. obliquus inferior and tales, which innervates the dentary and skin along the
the mm. rectus inferior and anterior. Cióse to the point anterior part of the mandible, and the ramus interman-
of división of the somatic rami, a smaller bundle of fibers dibularis, which supplies sensory fibers to the skin be-
belonging to the visceral afferent category forms the ra- tween the rami of the jaws and motor fibers to the mm.
mus communicans to the ramus ophthalmicus profundus intermandibularis and submentalis. In the caecilians, the
(C.N. V); after synaptic interruption in the ganglion cil- m. compressor glandulae orbitalis is innervated by the
iare, the fiber bundle innervates the intrinsic eye muscle, ramus mandibularis (Badenhorst, 1978), which is par-
the smooth m. sphincter pupillae. In caecilians having the tially anastomosed with the ramus maxillaris, A branch
eye covered by skin, the efferent nerves are reduced of the latter innervates the tentacular sheath in caecilians.
(Dermophis) or vestigial (Ichthyophis), whereas they are
absent ¡n caecilians in which the eyes are covered by C.N. VI (Abducens). This somatic motor nerve arises
bone. There is no connection of the oculomotor with the from the ventral surface of the medulla and exits the
trigeminal (C.N. V) in caecilians. neurocranium via the optic foramen in anurans and cae-
cilians and via a sepárate foramen abducentis in sala-
C.N. IV (Trochlearis). This somatic efferent nerve manders. In the orbit the nerve bifurcates, each ramus
originales ventromedially in the posterior part of the mes- innervating one of two eye muscles, the mm. rectus la-
encephalon, passes dorsally in a deep groove (cerebel- teralis and retractor bulbi. In caecilians, the nerve inner-
lomesencephalic fissure), crosses with its contralateral vates the retractor muscle of the tentacle, which is ho-
counterpart in the anterior medullary vellum, and exits mologous with the m. retractor bulbi of other amphibians.
the cranium via the optic foramen or a small, oblique In those caecilians having the eye covered by skin (e.g..
foramen anterodorsal to the optic foramen. This nerve Ichthyophis), the m. rectus lateralis is present and inner-
supplies a single eye muscle, the m. obliquus superior. vated by the abducens, whereas in those caecilians in
Francis (1934) discussed variation ¡n this nerve in sala- which the eye muscles are degenerated, that branch of
manders, noting that in Salamandra the nerve divides the abducens is absent.
before or after leaving the cranium; the smaller branch
innervates the m. obliquus superior, and the larger one C.N. VII (Facialis). The slender facial nerve origi-
anastomoses with the ramus ophthalmicus profundus nates on the ventrolateral surface of the medulla and exits
(C.N. V). In at least some caecilians with the eye covered the neurocranium through a foramen into the cavity formec
by skin (e.g., Dermophis, Hypogeophis), a thin trochlear by the tripodial attachment of the palatoquadrate (sala-
nerve is present, but it has not been observed in others. manders) or quadrate (anurans and caecilians). It is com-
posed of branchiomotor and visceral efferent fibers. The
C.N. V (Trigeminus). The trigeminal originates from facial nerve is closely associated with the auditory nerve
the lateral surface of the medulla and exits the cranium (C.N. VIII) within the neurocranium. Outside the neu-
via the large prootic foramen, which contains the Gas- rocranium the nerve passes anteriorly to the Gasserian
serian ganglion, from which branches of the trigeminal ganglion. From that point the ramus palatinus extends
nerve arise. The largest branch, the sensory ramus anteriorly and innervates the roof of the mouth; it is anas-
ophthalmicus profundus, contains somatic afferent fibers. tomosed with the ramus ophthalmicus profundus (C.N
This ramus actually arises from a second ganglion V) in salamanders and anurans. Also, the Harderian glar.;;
(ophthalmic ganglion) in caecilians; in all amphibians it in the orbit and the intermaxillary gland in the roof of
bifurcates into six major branches that innervate the skin the mouth are innervated by the ramus palatinus. The
on the snout, top of the head, and facial región, as well major part of the facial nerve consists of the truncus hy-
as penétrate the eyeball (superior and inferior ciliary rami). omandibularis, which exits between the otic and basal
 Integumentary, Sensory, and Visceral Systems
txocesses of the (palato)quadrate and gives rise to three glossopharyngeal-vagus ganglion (also apparently incor- 395
fatanches: (1) ramus alveolaris, sensory fibers that run porating the accessory nerve). The vagus consists of
aiong the lingual side of the lower jaw and innervate the branchiomotor and visceral efferent fibers; the latter con-
epnhelial lining of the floor of the mouth; (2) ramus mus- stitute the main peripheral path of the parasympathetic
cuians (or mandibularis), motor fibers that innervate the system. The branchiomotor fibers innervate three throat
— depressor mandibulae; and (3) ramus jugularis, motor muscles—mm. transversus ventralis, cephalodorsosub-
afoers that innervate the m. interhyoideus and (in sala- pharyngeus, and subarcualis rectus I. Sensory fibers sup-
manders) the m. subhyoideus. ply the mucosa of the mouth and pharynx. A ramus
auricularis provides afferent fibers to the tympanic región
C.N. VIH (Auditory). The auditory nerve is made up in anurans and salamanders. Various branches of the
pnmarily of special somatic afferent fibers, but it also con- main part of the vagus, the laryngeus ventralis. innervate
•2ins some efferent axons that exert an inhibitory influ- the smooth muscles and glands of the esophagus and
ence on the spontaneous activity of the vestibular afferent stomach, as well as the muscles of the lungs and heart.
ribers in anurans. Although these different fibers leave
—s lateral surface of the medulla, they maintain their C.N. XI (Accessorius). This small motor nerve emerges
rntegrity anteriorly to the torus semicircularis below the from the lateral wall of the medulla with the roots of the
optic ventricle of the midbrain. In salamanders and cae- vagus. It innervates a single pectoral suspensory muscle,
dHans, the auditory nerve is intimately associated with the m. cucullaris.
•acial nerve in the otíc capsule. In salamanders, the
rwo nerves have a common acoustico-facialis ganglion, C.N. XII (Hypoglossus). The primordia of this nerve
but in caecilians the auditory nerve seems to have a sep- are in the first and second spinal nerves, but this nerve
árate but poorly developed ganglion. In anurans, the au- contains fibers which represent the hypoglossal nerve in
ditory nerve remains distinct from the facial. The auditory amniotes; therefore, it can be considered with the cranial
nerve trifurcates and enters the auditory capsule vía three nerves. It exits from the spinal cord either through a for-
íoramina in salamanders, but has only two rami (and amen in Presacral I (salamanders and caecilians) or through
foramina) in anurans and caecilians. The ramus anterior an intervertebral foramen between Presacrals I and II
innervates the utriculi and ampullae of the anterior and (anurans). This nerve innervates the muscles associated
lateral cañáis (also the sacculus in anurans). The ramus with the tongue— mm. geniohyoideus, genioglossus, hy-
posterior innervates the ampullae of the posterior canal, oglossus, and rectus cervicis.
the papilla lagenae, and the papilla amphibiorum in all
three orders; in caecilians, this branch also innervates the Lateral-line Nerves. The lateral-line organs of larval
sacculus, and in anurans, the papilla basilaris. The sac- amphibians and certain ones that are aquatic as adults
culus is innervated by a ramus medianus in salamanders. (pipid frogs and oblígate neotenic salamanders) are in-
nervated by branches of cranial nerves. Except for those
C.N. IX (Glossopharyngeus). This small nerve con- groups mentioned, these nerves degenerate at meta-
sisüng of branchiomotor and visceral efferent and afferent morphosis. The ampullary organs and neuromasts of the
fibers arises directly in front of the first root of the vagus snout are innervated by the ramus lateralis anterior of
(C.N. X) on the lateral wall of the medulla. Both nerves the facial nerve (C.N. VII), and the other parts of the
exit the neurocranium via the postotic foramen imme- lateral-line system of the head by the ramus lateralis pos-
diately posterior to the otic capsule, where they form a terior (and its many branches) of the vagus nerve (C.N.
large glossopharyngeal-vagus ganglion. Except in caeci- X). The fibers of these nerves enter the medulla at the
lians, one branch of the glossopharyngeal passes ante- same point as those of the auditory nerve (C.N. VIII).
riorly to communicate with the facial nerve (C.N. VII).
Branchiomotor fibers of the ramus muscularis innervate Spinal Cord and Spinal Nerves
the m. subarcualis rectus I. The dorsal buccal mucosa is Details of the morphology and ultrastructure of the spinal
innervated by visceral afferent fibers of the ramus pha- cord in anurans were provided by Ebbesson (1976) and
ryngeus, and the tongue by the same kind of fibers in Sotelo and Grofova (1976), respectively. The gross mor-
the ramus lingualis, which also probably supplies special phology of the spinal nerves in anurans is based on
visceral afferent fibers to the taste buds of the tongue. Gaupp's (1896) work on Rana esculenta, whereas that
of Salamandra salamandra was described by Francis
C.N. X (Vagus). The origins of the vagus, glosso- (1934) and that of caecilians by H. Norris and Hughes
pharyngeal, and accessory nerves are difficult to distin- (1918).
guish in amphibians. Different authors recognize two to
four roots of the vagus, but apparently only two exist; Spinal Cord. The basic structure of the anterior part
the others represent the roots of the glossopharyngeal of the spinal cord is similar in the three living groups of
and accessory nerves. The vagus and glossopharyngeal amphibians. The cord is contained in the neural canal of
(C.N. IX) exit the neurocranium via the postotic foramen; the vertebrae and completely covered by bone of the
once outside the cranium the two nerves form a common imbrícate neural arches, except in some anurans, in which
MORPHOLOGY
nonimbricate neural arches leave portions of the spinal branches, as well as an anastomosis with the hypoglossal
cord exposed. The dorsal surface is formed by nuclei (C.N. XII). In all three groups, S.N. 1 innervates neck
where somatíc afferent fibers termínate; the lower part of musculature, and the hypoglossal fibers (C.N. XII) in-
the cord is formed by visceral efferent cells, below which nervate the tongue muscles.
are somatic efferent cells. Axons from the medulla extend Spinal nerves in the thoracic región are interconnected
for varying distances along the cord. For example, in to form the brachial plexus. In Salamandra, the plexus is
anurans, fibers from C.Nn. IX and X extend to the second formed primarily by S.Nn. 3 and 4 with some contribu-
and third spinal segments, from C.N. VIII to the sixth üons from S.Nn. 2 and 5. S.N. 2 in salamanders primarily
segment, and from C.N. V to the seventh segment. In ¡nnervates muscles of the pectoral girdle, but a branch
salamanders, fibers of Mauthner cells extend from the connects with S.N. 3. Prior to this fusión, S.N. 3 gives
medulla throughout the length of the spinal cord. off the ramus supracoracoideus which innervates pectoral
The spinal cord is uniform in size anterior to the sacrum muscles. S.N. 3 receives a branch from S.N. 4 and be-
except for the slight brachial and lumbar enlargements in comes the extensor nerve, which bifurcates into two
the regions of the brachial and sciatic plexuses in anurans branches that innervate the extensor muscles of the fore-
and salamanders. Postsacrally, the spinal cord diminishes limb. S.N. 4 has branches to thoracic muscles and to the
¡n size in salamanders. In anurans, the cord terminales m. rectus abdominis. After receiving a branch from S.N.
as such at the level of the sixth spinal nerve; succeeding 3, S.N. 4 gives off a branch to the m. pectoralis. Sub-
nerves extend independently in the neural canal, and a sequently there is a fine branch from S.N. 5, after which
slight, median cord terminales in the coccyx. the main branch of S.N. 4 enters the ventral part of the
forelimb as the brachial nerve to innervate the flexor
Spinal Nerves. Each body segment is supplied with a muscles.
pair of spinal nerves. In anurans, each nerve exits the The arrangement of nerves forming the brachial plexus
spinal cord intervertebrally, except the tenth and eleventh is different in anurans. In Rana, the plexus is formed by
(if present) which exit via foramina in the coccyx. Ver- S.Nn. 2 and 3, which have a connecting ramus; both
tebal fusión in some anurans (e.g., pipids and bufonids) nerves have branches to muscles of the pectoral girdle.
resulta in the nerves exiting via foramina in the fused The brachial nerve supplying the flexor muscles of the
vertebrae. In caecilians, the nerves exit via foramina in forelimb is derived from S.N. 2, and the extensors of the
the anterior vertebrae (vertebrae 1-3 in Typh/onectes to forelimb are innervated by S.N. 3. Thus, in the course
1-20 in ¡chthyophis) (M. Wake, 1980c). The first spinal of shortening the trunk región, a rearrangement of spinal
nerve always exits through a foramen in the first vertebra nerves has occurred, with S.N. 2 in anurans assuming
of salamanders, but the exits of the nerves in other ver- the brachial nerve that is a branch of S.N. 4 in salaman-
tebrae are variable (Edwards, 1976). In some salaman- ders.
ders (e.g., hynobiids), all other spinal nerves exit inter- Numerous experiments have shown that during de-
vertebrally, whereas in plethodontids all nerves exit through velopment peripheral nerves will develop in transplanted
foramen in the vertebrae, and members of some other limb buds (see Saxen and Toivonen, 1962, for review).
families are intermediate—some nerves are intravertebral For example, Detwiler (1927) showed that in salamander
and others are intervertebral. larvae a primordium transplanted to a more posterior
With the exception of the first spinal nerve (S.N. 1), portion of the body became innervated by the segment
which has no dorsal root in adults (dorsal root and gan- of the spinal cord juxtaposed to the transplant.
glion atrophy at metamorphosis), all spinal nerves have The sciatic or crural plexus of nerves that innervate the
a dorsal root with a large dorsal root ganglion and a hindlimb is formed in the vicinity of the sacral vertebra
ventral root which fuses with the dorsal root just periph- in salamanders. In Salamandra, which has 16 presacral
eral to the ganglion. At this point the small dorsal branch vertebrae, the plexus is formed by S.Nn. 16 and 17 with
of the spinal nerve passes dorsally to innervate the skin a contributíon from S.N. 15. The latter has an obturator
and muscles of the dorsal trunk (also, dorsal lymph sacs branch to the m. puboischiofemoralis, an iliohypogastric
in anurans). The large ventral branch of each spinal nerve branch to the muscles of the lateral and ventral body
innervates ventral and lateral skin and muscles of the wall, and a branch which anastomoses with S.N. 16.
body and the limbs. A ramus communicans extends from After receiving this branch, S.N. 16 gives off a branch to
each ventral branch to the sympathetic nerve cord. S.N. 17 and becomes the femoral nerve which innervates
The number of body segments, and therefore the the extensor muscles of the hindlimb. S.N. 17 exits from
number of vertebrae is highly variable in amphibians. the sacral vertebra and after receiving the branch from
Most anurans have only 10 pairs of spinal nerves, al- S.N. 16 becomes the sciatic nerve which innervates the
though more than 20 are present in tadpoles; all but 1 flexor muscles of the hindlimb. Small rami of S.Nn. 14
or 2 postsacral pairs atrophy during the absorptíon of the and 18 also make contributions to the sciatic plexus.
tail at metamorphosis. A small nerve, the occipital nerve, Three spinal nerves form the sciatic plexus in anurans.
anterior to S.N. 1 is uncommon in anurans and sala- In Rana, these are S.N. 7 which exits between Presacrals
manders, but in caecilians it has dorsal and ventral VII and VIII, S.N. 8 which exits between Presacral VIII
 Integumentary, Sensory, and Visceral Systems
2nd the sacrum, and S.N. 9 which exits between the tral nervous system via cranial nerves. Rami extend from 397
sacrum and the coccyx. S.N. 7 gives off an iliohypogastric the Gasserian ganglion of C.N. V and the glossopha-
branch to muscles of the lateral and ventral body wall; ryngeal-vagus ganglion of C.Nn. IX and X to the first
Éws. it seems to be homologous with S.N. 15 in Sala- sympathetic ganglion. A sepárate branch of C.N. X, the
•ncndra. S.Nn. 7-9 extend posterior under the m. ilio- laryngeus ventralis (= pneumogastric), innervates smooth
:occygeus to the base of the hindlimb, where they form muscles in the lungs, heart, and stomach.
TSC sciatíc plexus. S.Nn. 7 and 8 fuse, and this bundle Sympathetic and parasympathetic fibers are carried in
arastomoses with S.N. 9, which receives a branch from the same nerves, as are sensory fibers from the viscera
5 N. 10. Just after the fusión of S.Nn. 7 and 8, the cruralis to the central nervous system. The impulses of the sym-
-erve branches off and enters the hindlimb to innervate pathetic and parasympathetic fibers are antagonistic in
—-s extensor muscles. The main branch from the plexus their effects. For example, sympathetic impulses act to
s ríe sciatíc nerve, which with its many branches inner- hall peristalsis in the gut, to tighten the sphincters in the
vaies the flexor muscles of the hindlimb. gut, and to increase the rate of heartbeat; para-
Brachial and sciatic plexuses are absent in caecilians. sympathetic impulses have the opposite effects.
The ventral branches of the spinal nerves between the
rrachial and sciatic plexuses are rather uniform; each Interrelationships of Components
aves off branches to the lateral and ventral musculature The complexities of the nervous system are becoming
ar.d to the skin. The same general pattern exists through- better understood through electrophysiological, devel-
out the length of the body in caecilians and in the tail of opmental, and behavioral studies (see Llinás and Precht,
salamanders. In anurans, S.N. 10 fuses with a branch of 1976, for review). The reception of external stimuli has
S.N. 9 to form an ischiococcygeal plexus, from which been discussed in the previous sections: Integument; Sense
-•erves pass to the bladder, cloaca, oviducts, and poste- Organs. Reception of stimuli involves pathways from the
r.or lymphatic hearts. In primitive anurans, S.N. 11 anas- cranial or spinal nerves to correlation centers in the brain,
»moses with the ischicoccygeal plexus. which respond via motor pathways to the peripheral sys-
tem. Both sensory and motor pathways of the brain arise
Autonomic Nervous System from, and termínate on, a limited set of neurons in the
The autonomic nervous system is essentially the same in spinal cord. These spinal neurons form the basic reflex
rfie three living orders of amphibians. Detailed descrip- ares and are the only elements other than cranial nerves
aons of the system are given by Gaupp (1896) for Rana that transmit sensory information to the brain. Further-
escúdenla and by Francis (1934) for Salamandra sala- more, the efferent pathways of the brain can affect organs
mandra. A brief descriptíon of the system in caecilians is of the body only via these spinal elements.
provided by H. Norris and Hughes (1918). The pathways in the brain are numerous and complex;
The autonomic part of the peripheral nervous system they are discussed in detail by Nieuwenhuys and Opdam
innervates smooth muscles and glands; it has its own set (1976), Scalia (1976a, 1976b), and Sotelo (1976).
of ganglia sepárate from the central nervous system but
connected with it by communicating rami. Unlike the pe-
ripheral nerves of the central nervous system, motor neu- CIRCULATORY AND
rons do not extend from the central nervous system to RESPIRATORY SYSTEMS
the innervated organs. Instead, the neurons termínate in The transportation of oxygen and metabolic products
peripheral ganglia where they synapse with the dendrites through the body is dependen! on an effective system of
or cell bodies of the peripheral neurons that continué to ion binding, a pumping mechanism, and an efficient vas-
the organs. cular system. These are the blood, heart, and the blood
The autonomic nervous system consists of two parts— and lymph vessels, respectively. In contrast to other ver-
sympathetic and parasympathetic. Neurons of the sym- tebrales, amphibians have diverse modes of respiration—
pathetic system leave the central nervous system via spinal pulmonary, branchial, or buccopharyngeal. Each of these
nerves. A pair of sympathetic trunks ventrolateral to the modes involves different vascular systems to provide ef-
vertebral column receive neurons from the central nervous fective transport of oxygen from and carbón dioxide to
system via communicating rami to sympathetic ganglia the respiratory surfaces. Consequently, the circulatory and
along this trunk; numerous communicating fibers exist respiratory systems are discussed together.
between the two trunks. Synapses of the preganglionic
and peripheral neurons occur in these ganglia. Small nerves Blood
leave the sympathetic trunk and follow major arteries to The blood of amphibians is composed of plasma con-
the visceral organs. These nerves tend to form intricate taining erythrocytes, leucocytes, and thrombocytes. Ex-
plexuses, such as the solar plexus formed by branches cept for the erythrocytes, the other constituents are ca-
from Sympathetic Ganglia III-V and supplying the stom- pable of passing out of the blood vessels into the lymphatic
ach and adjacent parts of the alimentary canal. system. A thorough account of the structural and phys-
Neurons of the parasympathetic system leave the cen- iological properties of the blood in amphibians by Foxon
MORPHOLOGY
398 (1964) is summarized here. In adults, hematopoiesis takes Other Biochemical Changes). Hemoglobins in metamor-
place mainly in the spleen, but in anurans erythrocytes phosed amphibians have a lower affinity for oxygen than
also are formed in the marrow of the long bones at meta- larval hemoglobins, but they reléase oxygen more readily
morphosis and upon emergence from hibernaüon. Gran- at the oxygen tensions that prevail in the tissues of ter-
ular leucocytes are formed in the liver in some adult sal- restrial adults.
amanders and in the kidneys in proteids. Considerable The white cells are made up of agranular leucocytes
differences exist in sites of hematopoiesis, as do physio- (lymphocytes and monocytes) and granular leucocytes
logical properties of the blood, between larvae and adults (basophils, neutrophils, and eosinophils). Normally all of
(see Chapter 7). these cells are nucleated, but enucleated cells occur in
The red blood cells, erythrocytes, typically are nu- salamanders. The ratio of leucocytes to erythrocytes is
cleated and elliptícal. There is a great range in size, and 1:20-70. The size of leucocytes is relatively constant at
amphibians have the largest known erythrocytes. The a length of 30-32 qm. Foxon (1964) noted that com-
greatest length is 40-70 qm in oblígate neotenic sala- paraüve counts of the number of granular and agranular
manders; the largest are ¡n Amphiuma (erythrocytes are leucocytes is known for only a few species; he Usted
larger in larvae than in metamorphosed amphibians). In Bambino variegata as having 25% granular and 75%
anurans the length is 17.7—26.5 qm. Enucleated eryth- agranular leucocytes, and Salamandra atra as having 65%
rocytes (erythroplastids) are rare in anurans, but as many granular and 35% agranular leucocytes.
as 5% of the erythrocytes are enucleated in plethodontid Thrombocytes or spindle cells typically are nucleated,
salamanders, and erythroplastids make up 95% of the but enucleated cells (thromboplastids) have been re-
total in Batrachoseps attenuatus (Emmel, 1924). ported in some species of salamanders. These cells pre-
Counts of erythrocytes are roughly proportional to the sumably function like the platelets in mammals.
size of the cells. In Amphiuma means the erythrocytes
are 70 qm in length, and there are about 30,000/mm3, Heart and Aortic Arches
whereas comparable figures for some other species are: The structure and function of the heart have been dis-
Proteus anguinus 58 qm, 36,000/mm3; Nectuws macu- cussed in detail by J. Simons (1959), Foxon (1964), and
losus 54 qm, 51,000/mm3; Rana catesbeiana 25.5 qm, Kumar (1975). Usually the heart of amphibians has been
460,000/mm3; and Hy/a versicolor 20.7 qm, 900,0007 described as being composed of three chambers—two
mm3 (Szarski and G. Czopek, 1966). atria and one ventricle. However, a septum dividing the
Distinct biochemical differences exist between hemo- ventricle into right and left chambers is known in some
globins in larvae and those in adults (see Chapter 7: salamanders (Siren and Necturus) (J. Putnam and J. Dunn,

pulmocutaneous-| -carotid arch

arch -right atrium
-septum separating carotid and systemic
system i c channels in truncus arteriosus
arch
left atrium
anterior vena cava
ent ranee of
entranceto both pulmonary veins
pulmocutaneous
arches from cavum — pulmonary vein
pulmocutaneum ¡nteratrial septum
cavum aorticum
spiral valve ¡n conus
arteriosus dorsal atrioventricular
valve

ventricular musculature

Figure 14-17. Ventral view of the heart of an

anuran, Rana catesbeiana, partly sectioned in
the frontal plañe to show ¡nternal structure. The
circulatory pathway of oxygenated blood is
indicated by solid arrows and that of posterior vena cava
deoxygenated blood by broken arrows. Adapted
from W. Walker (1967).
 Integumentary, Sensory, and Visceral Systems
1978), and some caecilians (e.g., Ichthyophis and Hy- 399
«!>"«/»
pogeophis) have extensive trabeculae in the ventricle ¡nternal carotid-
iRamaswami, 1944; Lawson, 1966).
Although the hearts of the three living orders of am- external carotid
phibians are similar in gross morphology (Fig. 14-17),
there are differences in relative proportions and in the
intemal structure. In most salamanders and anurans the
ieft atrium is much smaller than the right, but in some common carotid
anurans (e.g., Xenopus) the two arria are about equal in ductus arteriosas
size. In caecilians the right atrium is much smaller than
the Ieft. Anurans have a complete interatrial septum, and pulmonary
the septum is fenestrated in caecilians and all salaman-
ders except Siren. In plethodontid salamanders the atrial
división consists of a membranous septum and a sino- truncus arteriosus
atrial valve (J. Putnam and D. L. Kelly, 1978). The sinus
venosus is divided into right and Ieft portions by inden- systemic artery
tations of the wall of the sinus or by a pair of transverse
valves in caecilians, and by constrictions of the inner wall
in anurans; there is no división of the sinus venosus in
salamanders. A sinoventricular fold is present in sala- conus arteriosus
manders but not in caecilians or anurans.
A conus arteriosus receives blood from the Ieft atrium
and becomes the median truncus arteriosus. Within the
conus is the spiral valve which is absent in at least some
plethodontid salamanders (Nel, 1970). The aortíc arches
divide from the truncus arteriosus. The truncus is short
in salamanders, exceedingly short in anurans, and greatly dorsal aorta
elongate in caecilians. The aortíc arches of adults are
derived from the visceral arches (V.A.) of larvae; the first Figure 14-18. Ventral view of the heart and principal arteries in
two visceral arches are lost. Only some salamanders have the anterior part of the body in a caecilian, /chthyophis glutinosus.
Redrawn from P. Sarasin and F. Sarasin (1887-90).
a full complement of aortic arches as adults. The carotid
arch (V.A. III) delivers blood to the head. The systemic
arch (V.A. IV) delivers blood to the body, including parts
of the head but excluding the pharynx and lungs (and temic arch persists in Herpe/e and Chthonerpeton and
to a varying extent the skin). The third arch (V.A. V) is only the Ieft in Hypogeophis. In some caecilians, such as
sepárate proximally but becomes confluent with the sys- ¡chthyophis, the right pulmonary artery is larger than the
temic arch in Salamandra and with the pulmonary arch Ieft. In Gegeneophis the Ieft pulmonary artery is absent;
in Necturus; it is small and not connected to other arches the small Ieft lung is supplied by a branch from the right
in Cryptobranchus and Amphiuma, and it is absent in pulmonary artery.
adult plethodontids (J. Putnam and Sebastian, 1977). The tissues of the heart obtain nutrients and oxygen
The pulmonary arch (V.A. VI) supplies the lungs and the from the blood passing through the organ. In addition,
walls of the pharynx; cutaneous branches also supply caecilians have a network of coronary veins covering the
skin, but this branch is reduced or absent in plethodontid ventricle; blood in these veins is derived from the cavity
salamanders. Only three arches persist in anurans; the of the ventricle and passes into the sinus venosus. Foxon
third arch is absent. (1964) suggested that these veins supply the muscular
Elongation of the body and reduction of the Ieft lung wall of the ventricle and that this system of coronary veins
have resulted in some major modifications of the aortic argües for a mixing of oxygenated and deoxygenated
arches of caecilians. Only two arches persist; the third is blood in the ventricle.
absent, and the carotid and systemic are fused. Usually Major modifications of the aortic arches take place dur-
two systemic-carotid arches and two pulmonary arteries ing metamorphosis with the change from branchial to
arise from the long truncus arteriosus. After the diver- pulmonary or cutaneous respiration; these changes are
gence of the carotid arteries, the systemic arteries extend more dramatic in the lungless plethodontid salamanders
posteriorly to merge into the median dorsal aorta in most and far less noticeable in the perennibranchiate neotenic
caecilians (Fig. 14-18). In others (e.g., Dermophis) the salamanders (Fig. 14-19). In larvae, the carotid arch sup-
two systemic arteries unite anterior to the heart to form plies the internal gills; it and the systemic and third arches
the dorsal aorta. Asymmetrical reduction of the arches is also supply the external gills. In crytobranchid and pro-
known in some genera. For example, only the right sys- teid salamanders a carotid duct exists between the affer-
MORPHOLOGY
400

ext car

aff br

-eff br
Figure 14-19. Metamorphic changes in branchial circulation in Desmognathus fuscus. A. Young larva,
ventral view of left side. B. Early metamorphic stage, ventral view of right side. The aortic arches are
identified by their visceral arch numbers; III, IV, V, and VI are carotid, systemic, third, and pulmonary
arches, respectively. Abbreviations: a = anastomoses (one for each branchial arch), aff br = afferent
branchial artery, d Bot = ductus Botalli, d car = ductus caroticus, dor a = dorsal aorta, eff br = efferent
branchial artery, ext car = external carotid artery, int car = interna! carotid artery, pul = pulmonary
artery, tr ar = truncus arteriosus. For the adult condition in salamanders, see Figures 14-20 and 14-21.
Adapted from McMuIlen (1938).

ent branches of the carotid and systemic arches. The thus, some oxygenated blood goes into that arch. The
pulmonary arch does not enter a gilí, but it may be con- slight differences in pressure among the aortic arches are
nected to the third arch by a duct (ductus Botalli). This insufficient to regúlate the flow of blood from the ventri-
duct is variably present in salamanders; it ¡s present in cle.
cryptobranchids, present or reduced in salamandrids and The foregoing account of the flow of blood in the heart
ambystomatids, and absent in proteids and plethodontids and aortic arches may be typical of terrestrial anurans,
(McMuIlen, 1938). During metamorphosis, anastomoses but a different pattern is evident in the aquatic Xenopus,
form between the efferent and afferent branches of each which relies more on pulmonary than on cutaneous res-
branchial arch; as the gills are resorbed, the anastomoses piratíon (De Graaf, 1957). In Xenopus blood returning
take over the entire blood flow. from the lungs passes to all parts of the ventricle. Upon
In amphibians blood leaves the single ventricle by routes ventricular contraction, the blood is distributed to carotid,
which may lead to the head, body, skin, or lungs (except systemic, and pulmocutaneous arches. Despite this ap-
in the lungless plethodonüd salamanders). Blood return- parent mixing in the ventricle, most blood returning to
ing from the head, body, and skin enters the left atrium the right atrium passes into the pulmocutaneous artery,
via the sinus venosus, and that from the lungs enters the which has a much lower diastolic pressure than the ca-
left atrium via the pulmonary vein (Fig. 14-17). The skin rotid and systemic arteries.
is an important respiratory surface in many amphibians, Studies on cardiac circulation in salamanders have
but blood that has been oxygenated there is mixed with provided conflicting interpretations. Segregation of oxy-
blood from the body in the right atrium. Thus, as em- genated and deoxygenated blood takes place in Am-
phasized by Foxon (1964), the circulatory arrangement phiuma tridacfylum, but no differential distribuirán occurs
in amphibians may be expected to show marked spe- in Salamandra salamandra or Trituras cristatus (Foxon,
cialization correlated with their peculiar respiratory meth- 1964). Differential distribution may be especially impor-
ods. tant in aquatic salamanders (e.g., Amphiuma and Siren)
The detailed description of cardiac respiration of Rana living in poorly oxygenated water, and presence of a
temporaria provided by J. Simons (1959) shows that little ventricular septum in Siren (also a complete interatrial
mixing takes place as blood passes from the atria to the septum) and in Necturus indicates that differential distri-
ventricle. The destination of any particular blood cor- bution may be complete in those salamanders. The pres-
puscle on leaving the ventricle is determined largely by ence of a sinoatrial valve that controls blood flow be-
its position in the ventricle. Thus, blood from the left side tween the atria seems to be associated with the loss of
of the ventricle passes up one side of the spiral valve in the pulmonary vein in plethodontid salamanders.
the conus arteriosus into the carotid arteries and the right No experimental data are available on cardiac circu-
systemic arch; simultaneously, blood from the right side lation in caecilians, but on the basis of morphology it
of the ventricle passes mainly up the other side of the seems most likely that mixing of oxygenated and deox-
spiral valve and ínto the left systemic arch. During the ygenated blood takes place in the ventricle. However,
early part of ventricular systole, a stream of blood flows the extensive ventricular trabeculae may function in par-
over the spiral valve from the cavum aorücum into the tial segregation of the blood as it is pumped out of the
cavum pulmocutaneum and on into the left systemic arch; ventricle.
 Integumentary, Sensory, and Visceral Systems
Vascular System lids (temporal artery) and to the roof of the mouth (man- 401
~~x arrangement of arteries and veins has been de- dibular artery), and (3) ophthalmic artery. The latter exits
-:-:¿; :or ñaña escalenta by Gaupp (1896), Xenopus the cranium via the oculomotor foramen; branches sup-
oe-cs by Millard (1941), and Salamandra salamandra by ply the eye, the eye muscles, and the eyelids. An anterior
---- ::¡ 1934); some general patterns in caecilians were branch of the ophthalmic anastomoses with a branch of
yven by Wiedersheim (1879). Obviously, only gross dif- the occipital ( = palatonasal) artery and enters the nasal
israr.ces and similarities ¡n the vascular systems of the capsule.
rree orders can be addressed here; furthermore, with Systemic system.—The systemic arches extend an-
~-= sxceptíon of the components of the aortic arches, terodorsally and then posteromedially to unite in the dor-
r~'¿ is known about the variation in the pattern of vessels sal aorta; this unification is anterior to the heart in sala-
•trun groups. For example, Millard (1941) pointed out manders and usually just posterior to the heart in anurans.
irferences in the vessels in the pelvic región between Several arteries diverge before the arches meet to form
X '.aeuis and R. esculenta, and Szarski (1948) noted nu- the dorsal aorta. The cutaneus artery supplies the thymus
—«rous interspecific differences in the vessels of the facial and parotoid región. In salamanders the pharyngeal ar-
2-.d pelvic regions among anurans. The presence of ade- tery supplies the jaw muscles and the hyoid muscles; the
r-a:e descriptions of only a few species is complicated mandibular branch supplies the lower jaw. In most anu-
irrther by a duplicity of ñames and inadequate knowl- rans these structures are supplied by the auricular branch
=cge of homologies. Consequently, the following com- of the cutaneus magnus artery which originales from the
—entary is very general and is intended only to serve as pulmonary arch. The occipital-vertebral artery in anurans
2_- introduction to the major aspects of the vascular sys- divides into an occipital artery that extends anteriorly into
the head and the vertebral artery that bifurcates and ex-
tends posteriorly on either side of the vertebral column.
Arteries. As noted in the preceding discussion of the The occipital is the same as the palatonasal in salaman-
-eart and aortic arches, profound differences exist in the ders, in which it and the vertebral artery have sepárate
-.umber and arrangement of the aortic arches. The ar- origins from the systemic arch. The occipital has several
teries are discussed in relatíon to the aortic arches from branches: (1) pharyngeal to walls of the pharynx, (2)
•.vhich they are derived (Fig. 14-20). pterygoid to the roof of the mouth, (3) maxillopalatíne
Carotid system.—The left and right common carotids to the roof of the mouth and posterior región of the
origínate from their corresponding systemic-carotid arches maxilla, and (4) anterior and posterior palatines to the
in caecilians, or from the persistíng arch in those taxa in palate. A final branch of the occipital artery is the orbi-
which one of the arches has been lost. The common tonasal, which passes below the eye muscles in salaman-
carotids origínate from their corresponding arches in sal- ders and dorsal to those muscles in anurans. The orbi-
amanders and primitive anurans (leiopelmatids, discog- tonasal has three nasal branches to the nasal capsule,
lossids, and pipids); both carotíd arteries origínate in as- two maxillary branches to the upper jaw, and an anterior
sociatíon with the left systemic arch in other anurans. orbital branch which anastomoses with a branch of the
Immediately before the divergence of the interna! and ophthalmic branch of the internal carotíd artery. Poste-
external carotíd arteries there is an enlargement of the riorly, the vertebral arteries have numerous small branches
common carotíd in anurans and salamanders. This en- to the dorsal trunk musculature and to the skin on the
largement, the so-called carotíd gland, contains a mem- dorsum.
branous labyrinth and apparently functions to divert blood The arteries supplying the organs in the coelom nor-
into the external carotíd artery which diverges at an ob- mally all emerge from the dorsal aorta. The large coe-
tuse angle from the common carotid. No carotíd gland liaco-mesenteric artery originales just posterior to the
exists in caecilians, in all of which the two carotid arteries confluence of the systemic arches; however, it emerges
diverge in an anterior direction. from the left systemic arch in most anurans but from the
The external carotid artery delivers blood to the mus- dorsal aorta in leiopelmatids, discoglossids, and pipids.
cles of the tongue and the floor of the mouth via four This artery has many branches that have been given di-
major branches: (1) muscular artery to the mm. rectus verse ñames and seem to be variable in their arrange-
cervicis and interhyoideus posterior, (2) thyroid artery to ment; the terminology of Francis (1934) is followed here.
the thyroid gland, (3) sublingual artery to the the típ of The three major branches are: (1) gastrico-linealis to the
the snout where branches go to the tongue and the spleen and dorsal wall of the stomach, (2) duodeno-
m. geniohyoideus, and (4) lingual artery to the tongue. hepatic with many branches to the liver, duodenum, ven-
The internal carotid artery supplies the upper jaw and tral wall of stomach, and gall bladder, and (3) duodeno-
cranium, which it enters by way of the carotid canal and pancreatic to the páncreas and duodenum. Four to eight
the basicranial fenestra. The major branches are: (in Salamandra) anterior mesenteric arteries origínate from
(1) cerebral artery with many branches supplying the the dorsal aorta and supply the distal part of the small
chorioid plexuses of the brain, (2) lateral pretrosal intestine, and three posterior mesenteric arteries deliver
(= stapedial) artery to the ear with branches to the eye- blood to the large intestine.
MORPHOLOGY
402
mandibular
-maxillary
• ophthalmic
exterior carotid

interior carotid
pulmonary
subclavian

vertebral

epigastrio

anterior oviducal
coeliaco-mesenteric
dorsal aorta

renal-
-femoral
Figure 14-20. Semidiagrammatic
ventral views of the arterial system In
amphibians. A. Salamandra ischiadic
salamandra, left side (adapted from
Francis, 1934). B. Xenopus laevis,
right side (adapted from Millard, caudal
1941). Only major vessels are
labeled.

The arteries supplying the urogenital system consist of cutaneous system. In both groups it continúes posteriorly
numerous srnall vessels to the gonads, oviducts, and kid- to connect with the femoral artery.
neys. Each kidney is supplied by numerous, short renal The arrangement of arteries in the pelvic región and
arteries from the dorsal aorta to its dorsal surface, whereas hindlimb differs from the pattern in salamanders. The
its ventral surface is supplied by the superficial renal ar- dorsal aorta bifurcates to form a pair of common iliac
tery which emerges from the posterior oviducal artery just arteries in anurans, whereas a trifurcation includes a cau-
posterior to the kidney. Three oviducal arteries deliver dal artery in salamanders. After giving off the femoral
blood to the anterior, middle, and posterior parts of the artery, which has an anastomosis with the epigastric ar-
oviduct. The mesial and posterior oviducal arteries origí- tery, the common iliac continúes on as the ¡schiadic ar-
nate from the dorsal aorta, whereas the anterior one tery. This is the major vessel entering the hindlimb; pos-
emerges from the dorsal aorta, subclavian artery, or ver- terior and ventral thigh muscles are supplied by a major
tebral artery. The oviducal arteries are srnaller in males branch, the cutaneus femoral artery.
in which they supply the Müllerian ducts. Four or five Pulmocutaneous system.—In caecilians and sala-
ovarían (or spermatic) arteries diverge from each side of manders (except plethodontids) the pulmonary arches
the dorsal aorta and carry blood to the gonads and fat curve posterolaterally from the truncus arteriosus to enter
bodies. the lungs. Along this short route, dorsal and ventral
A large subclavian artery branches off from each sys- esophageal arteries emerge and pass anteriorly to deliver
temic arch in anurans or from either side of the dorsal blood to the floor of the mouth, pharynx, and esophagus
aorta just posterior to the heart in salamanders. Numer- before the major vessel, the pulmonary artery, turns to
ous small branches deliver blood to the muscles of the enter the lungs. In lungless plethodontid salamanders in
shoulder región, and a major branch, the brachial artery, which the pulmonary arch is present, the pulmonary ar-
supplies the forelimb. The epigastric artery branches off tery supplies the skin of the neck and dorsum and in
at the point of origin of the brachial artery in salamanders; some species it anastomoses with the epigastric artery.
it supplies the ventral pectoral región and the ventral The pulmonary arch in anurans is much more important
body wall. In anurans this artery is part of the pulmo- in delivering blood to the skin. The main vessel, the pul-
 Integumentary, Sensory, and Visceral Systems
403
-mandibular
orbitonasal-
brachial
facial
external jugular
internal jugular
cutaneus magnus
subclavian
pulmonary
posterior cardinal
brachial
hepatic
postcava I
hepatic portal
oviducal
lateral
ventral abdominal
Jacobson's
femoral
ischiadic Figure 14-21. Semidiagrammatic
ventral views of the venous system in
amphibians. A. Salamandra
cutaneus femoral salamandra, left side (adapted from
Francis, 1934). B. Xenopus laevis,
right side with position of heart
outlined (adapted from Millard,
1945). Only major vessels are
caudal labeled.

monary artery, delivers blood to the heart, but the large exceedingly short because the juncture of the veins on
cutaneus magnus artery originates from the pulmocuta- the left side is adjacent to the sinus venosus; on the other
neous arch and supplies the skin of the dorsal and lateral hand, the right precaval extends across the dorsal surface
body wall; a branch of the cutaneus magnus, the auricu- of the heart to the dextral córner of the sinistrally offset
lar artery, supplies the jaw muscles, hyoid muscles, and sinus venosus.
tíssues of the lower jaw. Three major veins, the internal and external jugulars
and the subclavian, enter the precaval vein (Fig. 14-21).
Veins. The venous system is more variable, especially A postcardinal vein is present in larvae and in adults of
peripherally, than the arterial system. A major difference caecilians, salamanders, and leiopelmatid and discoglos-
exists among the living orders with respect to the recep- sid frogs. The internal jugular receives many veins drain-
tacle of the systemic veins, the sinus venosus, from which ing the palate, brain, and the orbital, nasal, and auditory
blood passes into the right atrium via the sinoatrial open- regions; the vertebral vein collects blood from the mus-
ing on the dorsal side of the atrium. The sinus venosus cles of the neck and drains into the internal jugular. The
is transversely elliptícal in caecilians; the left portion is external jugular vein with its major confluents (facial, lin-
separated from the slightly smaller right portion by an gual, and thyroid veins) collects blood from the muscles
internal indentation of the walls or by transversely situ- of the head and tongue and the thyroid gland. The sub-
ated valves. The sinus in salamanders is approximately clavian vein collects blood from the forelimb via the bra-
triangular and is situated to the left of the midline; it is chial veins, from the muscles and skin of the trunk via
the same shape but medial in position in anurans. the anterior epigastric and lateral veins; the anterior part
Systemic veins.—The veins that enter the sinus ven- of the latter also is known as the cutaneus magnus vein.
osus from all regions of the body are grouped into this The postcardinal veins (when present) origínate as a sin-
category. The sinus venosus receives three major veins, gle vessel from the posterior part of the postcaval vein;
the postcaval which enters the posterior part of the sinus, shortly after the origin a bifurcaüon results in the two
and the paired precaval veins (ducts of Cuvier) which postcardinals that pass anteriorly on either side of the
enter the lateral corners of the sinus. The left precaval is dorsal aorta to enter the precaval veins. The postcardinals
MORPHOLOGY
404 provide an altérnate route for blood from the región of lymph hearts are valves that restrict a unidirecüonal flow
the kidneys to the sinus venosus. of lymph in the vessels. Lymph is received in the hearts
The postcaval originales near the posterior end of the from the cutaneous network and from branches from the
kidneys by the fusión of a large renal vein from each subvertebral vessels that collect lymph from the body
kidney. The postcaval receives various vessels from the cavity. A central lymph heart associated with the truncus
kidneys and gonads and passes through the liver to the arteriosus receives lymph from the head and neck and
sinus venosus. In anurans, right and left branches of the delivers it to the lingual vein.
hepatic vein from corresponding lobes of the liver coa- Caecilians differ from salamanders by having more trian
lesce before entering the postcaval vein. 200 lymph hearts situated intersegmentally under the skin
Hepatic-portal system.—A major vessel, the ventral (H. Marcus, 1908); these hearts pump lymph into inter-
abdominal vein, is formed by the coalescence of veins in segmental veins.
the pelvic región. The pelvic veins fuse to form the ventral Anurans have few lymph hearts; an anterior pair is
abdominal in anurans, but in salamanders the coalesc- located beneath the scapulae, and one to five posterior
ence also includes the median cloacal and posterior vesi- pairs are situated along the coccyx. Anurans differ from
cle veins from the cloaca and bladder, respectively. The other amphibians by having extensive subcutaneous lymph
ventral abdominal vein passes forward along the ventral spaces. These are separated by fine septa and are most
midline and thence through the liver to the postcaval. In extensive in aquatic anurans. The spaces store water ab-
the región of the liver it receives vesicles from the gall sorbed from the environment. Cárter (1979) proposed
bladder and the portal vein with branches from the stom- that excess water is excreted by the posterior lymph hearts
ach and intesünes. pumping water from the lymph spaces into the renal por-
Renal-portal system.—The veins of the hindlimb tal vein and thence to the kidney.
combine (also with the caudal vein in salamanders) to
form the paired Jacobson's veins which pass anteriorly Respiratory System
on the dorsolateral surface of the kidney, from which they Amphibians have diverse modes of respiraüon. Larvae
receive many small vesicles. Jacobson's vein also re- have gills that are the primary respiratory structures, but
ceives blood from the oviducal vein and trien passes an- cutaneous respiration also takes place (see Chapter 6).
teriorly to enter the postcaval vein. Most postmetamorphic amphibians have lungs; these and
There are distinct differences in the veins of the pelvic the buccopharyngeal surfaces are the internal respiratory
región and hindlimb among anurans and between anu- structures; however, considerable gas exchange takes place
rans and salamanders. For example, in Salamandra and cutaneously in terrestrial amphibians (see Chapter 8).
Xenopus the major vessel from the hindlimb is the is- Herein the structures associated with buccopharyngeal
chiadic vein, whereas the femoral vein is the major vessel and pulmonary respiration are discussed.
¡n Rana. Also, there are differences in the anastomoses
of the femoral and Jacobson's veins. Nares. The nostrils (external nares) and the narial duct
Pulmonary system.—The pulmonary veins arise from are intimately associated with the olfactory system (see
the mesial surfaces of the lungs, fuse near the midline, earlier section: Sensory Receptor Systems). The narial
and enter the left atrium. A few small vesicles are received duct opens into the buccal cavity via the choana (internal
from the esophagus. naris). The nares are closed by means of smooth muscles
in salamanders and caecilians; in anurans the nares are
Lymphatic System closed by an upward swelling of the m. submentalis (Gans
A third series of vessels, the lymphatics, extends through- and Pyles, 1983).
out the body of amphibians; these vessels collect blood
(exclusive of erythrocytes) that seeps through the walls Buccopharyngeal Cavity. The mouth and pharynx
of the capillaries and return it to the veins. The intestinal are lined with mucoid and ciliated epithelium that is highly
lymphatics also collect fats, which are not absorbed by vascularized. In the floor of the pharynx is a longitudinal
the capillaries entering the veins. slitlike aperture, the glottis, which leads to the larynx. The
The lymphatic system of Salamandra was described glottis is bounded by the arytenoid cartilages, and the
by Francis (1934), who noted the fine subcutaneous net- glottis is opened and closed by the mm. dilatator laryngis
work of vesicles, especially laterally on the body and the and constrictor laryngis, respectively.
lymphatic sinuses in the head and at the bases of the
limbs. The subcutaneous lymphatics in salamanders empty Larynx. The larynx is a narrowly triangular chamber;
into the postcardinal veins or various cutaneous vessels. an elongated posterior tube, the trachea, is present in
The visceral lymphatics parallel the digestive tract and salamanders, caecilians, and pipid frogs. The larynx is
empty into the subclavian veins. Lymph is pumped through supported by a series of semicircular cartilages, the so-
the system by a series of contractile vesicles, the lymph called lateral cartilages. The anterior pair is modified as
hearts. In Salamandra there are 15 pairs of lateral hearts— the arytenoid cartilages, which support the glottis and are
4 postsacrally and 11 presacrally. Associated with the an integral part of the sound-production system in anu-
 Integumentary, Sensory, and Visceral Systems
rans isee Chapter 4). The second pair, the cricoid carti- ticated experiments by De Jongh and Gans (1969) on 405
age. forms a complete ring in most adult amphibians. A Rana catesbeiana have demostrated that all amphibians
•Jsrtral evagination forms a tracheal lung in some cae- studied breathe by means of a force-pump mechanism.
-fe=>ns (Typh/onectes compressicauda and Uraeotyphlus Acüon of the throat musculature elevates and depresses
axyurus); in these caecilians the ciliated tracheal mucosa the floor of the buccal cavity; this is analogous to the
s replaced by respiratory epithelium and the walls of the pistón of the pump. When the nostrils are open and the
racheal lung are infiltrated by cartilage and served by buccal floor is depressed, air is drawn into the buccal
—€ tracheal artery. In salamanders, caecilians, and pipid cavity; closure of the nostrils and elevation of the buccal
fcogs. the trachea bifurcates posteriorly into the bronchi, floor concomitant with the opening of the glottis forces
nsired short tubes with ciliated epithelium leading into air into the lungs. The cycle is reversed by the depression
±e lungs; bronchial tubes are absent in other anurans. of the buccal floor while the glottis is open and the nares
are closed; air is drawn out of the lungs into the buccal
Lungs. Basically the lungs are paired organs. Although cavity. Subsequent closure of the glottis and opening of
±cy are variable in size (small in Ascaphus) and espe- the nares combined with elevation of the buccal floor
dally large in some aquatic taxa (e.g., pipids and Tel- forces air out of the mouth. This mechanism is modified
"-.orobius), paired lungs are invariably present in anurans. during vocalization in anurans (see Chapter 4).
Ir. pipids the lungs are reinforced by cartilage. Most sal- Pulmonary respiration and buccopharyngeal respira-
2-T.anders (including the oblígate neotenes) have well- tion are complemented by cutaneous respiration in most
¿eveloped, paired lungs, but in some taxa that inhabit terrestrial amphibians, and by cutaneous and branchial
rr.ountain streams (e.g., Salamandrina and Rhyacotriton) respiration in many aquatic amphibians. The differentíal
ríe lungs are greatly reduced in size. Lungs are absent rates of gas exchange are dependent on the degree of
in all plethodontid salamanders. The lungs of caecilians capillarity of the different respiratory surfaces as well as
are extremely elongate; the right and left lungs are ap- temperature and moisture of the skin. These functional
proximately equal in length in some caecilians (e.g., Ty- aspects of respiration are discussed in Chapter 8.
phlonectes and ¡chthyophis monochrous). In most cae-
cilians the left lung is reduced, in some to about 10% of
the length of the right lung, and the left lung is absent in UROGENITAL SYSTEM
ü'raeotyph/us narayani (Baer, 1937). The excretory and reproductivo systems are closely as-
Structurally, the lungs of terrestrial salamanders are sociated in amphibians, as they are in all vertebrales,
conical sacs, more or less pointed posteriorly. The pul- although these structures origínate from different embry-
monary membrane is folded to form internal septa, and onic tissues (see Chapter 7). The urogenital system of
each lung has two longitudinal compartments, one con- salamanders was described in detail by Francis (1934),
taining the pulmonary artery and the other the pulmo- who based his work on Salamandra salamandra. Bhaduri
nary vein. The septa are highly vascularized and covered (1953) and Bhaduri and Basu (1957) provided compar-
with a thin epithelium except along their inner edges where ative descriptions of the system in anurans. The com-
ciliated and mucous cells cover the sheaths of smooth parative morphology of the system in caecilians was de-
muscle. In oblígate neotenic salamanders and some aquatic scribed in detail by M. Wake (1968,1970a, 1970b, 1972),
salamandrids (e.g., Notophthalmus and Triturus) the lungs and early development was treated by Fox (1963).
have few septa and are comparatively poorly vascular- In this section the morphology of adults is described
ized. In caecilians the elongate lung is infiltrated by car- (Fig. 14-22). The ontogeny of the urogenital structures
tilage; the inner surface is divided by a network of blood is covered in Chapter 7. The production of sperm and
vessels, connecüve üssue, and smooth muscle which form ova is discussed in relation to sexual cycles in Chapter
alveoli. The lungs of terrestrial anurans are short but sim- 2, and kidney function is discussed ¡n relation to water
ilar in structure except that they lack cartilage (except and ion balance in Chapter 8.
pipids) and the septa form more and smaller chambers.
In aquatic amphibians (especially oblígate neotenic sal- Kidneys
amanders, some adult newts, pipid frogs, and possibly The kidneys in adult amphibians are paired structures
typhlonectid caecilians) the lungs seem to functíon more lying on either side of the dorsal aorta. They develop
as hydrostatic organs than as respiratory organs. Some from larval nephrostomes. In caecilians, anterior and pos-
of these aquatic salamanders (e.g., Cryptobranchus, Am- terior nephrostomes persist in the formation of the kid-
phiuma, and Triturus) breathe air through the nares, but ney; thus, caecilians have an opisthonephric kidney, in
Siren and Necturus take air in through the mouth (Atz, which some evidence of segmentatíon is retained in adults.
1952), as pipid frogs do commonly. The anterior part of the larval kidney (pronephros) is lost
in adult anurans and salamanders; only the middle and
Breathing. Observations and experiments on sala- posterior nephrostomes persist in adults, which therefore
manders and anurans by Willem (1924), on a caecilian have a mesonephric kidney (Fig. 7-3).
(Siphonops annu/aíus) by Mendes (1945), and sophis- The gross morphology of the kidneys differs in the
MORPHOLOGY
406 B
infundibulum

lung
Mullerian duct

postcardinal vein
fat body
dorsal aorta
fat body mesorchium
mesovarium testis

ova
efferent
postcaval vein ductules
Wolff ian duct
oviduct

collecting
ducts

kidney

urmary bladder
cloaca

infundíbulum

mesorchium
mesovarium testis
Figure 14-22. Ventral views of
efferent
postcaval vein ductule
urogenital structures in salamanders
and anurans. A. Salamandra kidney
salamandra, female. B. Same, male.
C. Rana catesbeiana, female. kidney •Wolffian duct
D. Same, male. Some structures Wolffian duct
have been omitted from one side of urinary bladder
each drawing. A and B adapted from
Francis (1934); C and D adapted
from W. Walker (1967). cloaca

three living orders of amphibians. The kidneys are long merulus is surrounded by an expanded end of a kidney
and slender in caecilians, in which they extend from the tubule; this structure, Bowman's capsule, ¡s the major site
región of the heart nearly to the cloaca. In hynobiid and of filtration. The kidney tubules extend laterally through
cryptobranchid salamanders, the kidneys also are eion- a capillary network and carry uriñe to the Wolffian duct.
gate and there is no obvious sexual dimoiphism in shape. The capillary network is made up of vessels derived from
In other salamanders the kidneys are proportionately the renal portal vein, which enters the posterior end of
shorter, and those in males are narrow anteriorly. The the kidney; blood leaves the kidney via the renal portal
kidneys in anurans vary from long and slender, six to vein to the postcava. In males, the anterior kidney tubules
eight times as long as broad (e.g., Ascaphus, Heleo- usually receive the efferent tubules from the testes. The
phryne, and Dendrobates) to only about three to four kidney tubules and glomeruli are essentially uniform in
times as long as broad (most anurans). size throughout the length of the kidney in both sexes in
The kidney is highly vascularized from numerous renal caecilians, whereas in males of many salamanders and
arteries from the dorsal aorta which branch to form in- anurans the anterior nephric units are modified in that
numerable clusters of capillaries or glomeruli. Each glo- functional glomeruli and distal tubules are absent. In these
 Integumentary, Sensory, and Visceral System
males the tubules in the anterior part of the kidney func- neys. The ovary consists of a thin sheath of connective 40
tion solely for sperm transport. tissue, the ovisac, enclosing the ovarían follicles. Ovarían
development is discussed in Chapter 2. Rupture of the
Gonads ovisac releases the ripe ova into the coelom. The epithe-
lium of the coelom is ciliated, and ciliary action moves
Testes. The paired testes are attached to the kidneys
the eggs anteriorly to the opening of the oviduct.
by a membrane, the mesorchium, which supports the
efferent ductules from the testes to the kidneys. The testes
increase in size during the breeding season, and in some Urogenital Ducts
species of anurans they become pigmented. In anurans In addition to the kidney tubules and efferent ductules
the testes usually are spheroid or ovoid structures that from the testes, two major longitudinal ducts are present
are ventral to the anterior half of the kidneys, but in some in the urogenital system. The Wolffian duct originating
species the testes are much larger, especially in length, on the lateral edge of the kidney carnes uriñe (and in
and extend nearly to the posterior end of the kidneys. males, sperm) to the cloaca. Normally, each Wolffian
The testes in anurans are not lobed as they are in many duct enters the cloaca separately in salamanders, caeci-
salamanders, in at least some of which lobes are added lians, and most anurans. However, the ducts unite and
with successive annual breeding cycles (see Chapter 2). enter the cloaca through a single aperture in diverse kinds
The testes in caecilians are greatly elongate and lobed; of anurans (e.g., E/eutherodacty/us, Heleophryne, Pa-
the lobes are connected by a longitudinal duct. The num- chymedusa, Kassina, and many species of Bu/o). Sexual
ber of lobes varíes from 11 to 20 in species of Ichthyophis dimorphism in the fusión of the ducts was noted by Bhaduri
to only one in /diocranium russe/i and some individuáis (1953), who also noted the formation of a urogenital
of Dermophis mexicanus (M. Wake, 1968). In some spe- sinus upon fusión of the ducts in Ascaphus truei and
cies of caecilians the anterior lobes are largest; in others Rhinophrynus dorsalis.
the posterior lobes are largest; and in still others the lobes In some anurans the lower part of the Wolffian duct is
are more or less uniform in size. expended into a seminal vesicle; according to Bhaduri
Spermatogenesis occurs in locules in the testes, and (1953) and Bhaduri and Basu (1957), the seminal vesicle
sperm are transported through collecting ducts into a lon- may be seasonal in appearance. The portion of the Wolf-
fian duct adjacent to the kidney is enlarged and has a
gitudinal duct in the testes and then to the kidney via
glandular epithelium in species of Rhacophorus, Poly-
efferent ductules (vas efferentia). A longitudinal testícular
duct is absent in some salamanders. The efferent ductules pedates, and Chiromantis that have been examined.
Bhaduri (1932) suggested that the glandular epithelium
join nephric collecting tubules which empty into the Wolf-
provided secretions that were used in the construction of
fian duct. The number of efferent ductules is highly var-
arboreal or terrestrial foam nests (see Chapter 5). Iwa-
iable and usually is correlated with the size of the testis
sawa and Michibata (1972) found that sperm were stored
and the number of lobes. For example, in caecilians there
are usually 1 to 5 ductules per lobe, but some large an- in the coiled glandular part of the duct adjacent to the
terior lobes may have more than 5 ductules. Salaman- kidney in species of Rhacophorus that constructed foam
ders and anurans usually have 4 to 12 ductules associ- nests.
ated with each testis, but only 2 are present in proteid The oviducts lie parallel and lateral to the kidneys; they
are nearly straight in caecilians, slightly convoluted in sal-
salamanders and discoglossid frogs (Noble, 1931b). Al-
amanders, and greatly convoluted in anurans. The open-
though sperm usually are transported to the cloaca in the
ing of the oviduct, the infundibulum (= ostium), is cil-
Wolffian duct, the nephric collecting tubules pass directly
into the cloaca in some primiüve salamanders (Noble,
1931b). For example, in both sexes of Andrios japonicus
and in male Hynobius /¡chenatus the collecting tubules
empty independently into the cloaca; in female H. \\ch-
postcaval veín
enatus some of the tubules enter into the cloaca and
others into the Wolffian duct, whereas in male Onycfio-
dacty/us some tubules form a common duct to the cloaca
and others empty into the Wolffian duct.
In larval bufonids, the anterior end of each developing
gonad has a growth of ovarían tissue. This is retained in
adult male bufonids as the Bidder's organ, which may
be a peripheral or lateral band or an anterior cap on the
testis (Fig. 14-23). kidney

Ovarles. The paired ovaries are suspended by a mem- Figure 14-23. Ventral view of the left urogenital system of a male
brane, the mesovarium, from the mesial side of the kid- Bufo woodhousti showing the position of Bidder's organ.
MORPHOLOGY
408 iated and located in the vicinity of the lung. The walls of these glands and the associated structures are dealt with
the oviduct contain a smooth muscle layer in a circular in the discussion of internal fertilization given in Chap-
pattern of fibrous and elastic tissue. The lumen is lined ter 3.
with ciliated epithelium. During gestation in viviparous
caecilians and anurans, the epithelial cells secrete sub- Fat Bodies
stances that nourish the fetuses (see Chapter 2). Also, Fat bodies associated with the gonads are characteristic
secretory glands in the lower part of the duct in oviparous of all amphibians. In salamanders the fat bodies are in
species secrete mucoids that form the egg capsules (see the form of longitudinal strips between the gonads and
Chapter 7). the kidneys. In anurans the fat bodies are in the form of
Homologues of the oviducts, the Müllerian ducts, per- many fingerlike projections aggregated at the anterior end
sist in males of a few species of anurans, but they ap- of the gonads; the bodies are larger and more pointed
parently have no functíon. These ducts are comparatively in males than in females. Caecilians usually have nu-
well developed in male caecilians, in which the posterior merous leaflike fat bodies that extend in a series on each
part of each duct has glandular epithelium, the secretions side of the body from the liver to the cloaca. The fat
of which apparently aid in sperm transport for internal bodies of anurans and caecilians are suspended from the
fertilization (M. Wake,1981; see Chapter 3). body wall by a dorsal mesentery which is fused with the
gonadal mesentery (mesovarium or mesorchium). The
Urinary Bladder fat bodies in salamanders are suspended from the gon-
The urinary bladder is a ventral outgrowth of the cloaca. adal mesenteries. Fat bodies are composed of typical adi-
Its single opening into the cloaca is controlled by a pose tissue consisting of large cells, each with an oil vac-
sphincter. The lining of the bladder consists of smooth uole. A thin, fibrous connective tissue surrounds each fat
epithelium separated by a submucosal layer from longi- body; the individual coats of connective tissue fuse with
tudinal smooth muscle. The latter lies inside bands of the mesentery.
circular muscle. These muscle layers allow for the great According to Noble (1931b), fat bodies are a source
distensión of the bladder when it is filled with uriñe. of nutrients for the gonads. The bodies are largest just
The bladder is cylindrical or bicornuate in salaman- before hibernation and smallest just after breeding.
ders, slightly bilobate in other salamanders and some
anurans, and usually deeply bilobate in caecilians, a group
in which the proportional sizes of the lobes is sexually DIGESTIVE SYSTEM
dimorphic in some species. Other modifications of the The alimentary canal and associated organs of amphib-
bladder in caecilians, such as the degree of mesenteric ians commonly are the first aspects of internal anatomy
attachment and presence of a m. rector cloacae, seem to viewed by students of biology. A general account of the
be associated with the presence of a phallodeum and digestive system in amphibians was given by Noble
internal fertilization (M. Wake, 1970b). (193Ib), and good descriptions of the system are avail-
able for Rana escalenta (Gaupp, 1896), Salamandra sal-
Cloaca amandra (Francis, 1934), andNecturus maculosus (I. Ol-
The cloaca is the common receptacle for the alimentary sen, 1977). A comprehensive account of the microstructure
canal, Wolffian ducts, oviducts, and the bladder. The al- and functional aspects of the system was provided by
imentary canal enters the cloaca anteriorly, the bladder Reeder (1964). The larval gut and changes during meta-
ventrally, and the ducts dorsally. A sphincter surrounds morphosis are discussed in Chapter 7.
the external opening of the cloaca. Urogenital papillae
are associated with the openings of the ducts in some Structure
species of caecilians and salamanders. The cloaca is a The basic structure of the system is fundamentally similar
relatively simple structure in anurans and primitive sala- in all three groups of living amphibians, except that the
manders. The lining of the cloaca is composed of ciliated, organs are more compressed anteroposteriorly in anu-
columnar epithelium, except cilia are lacking in pouches rans than they are in salamanders and they are attenuate
present in some caecilians. A submucosal layer is made in caecilians (Fig. 14-24).
up of fibrous connective tissue and is bounded by a layer
of circular muscle and an outer layer of longitudinal mus- Buccal Cavity. The mouth contains the teeth (absent
cle which is continuous with that of the intestine. in some anurans), tongue (absent in pipid frogs), and
In contrast to the rather simple condition in anurans glands. The role of the teeth and tongue in obtaining
and primitive salamanders, the cloaca in those salaman- food is discussed in Chapter 12. The buccal cavity is lined
ders having internal fertilization is modified by the pres- with oral mucosa variously elaborated as unicellular and
ence of sets of glands that are sexually dimorphic in struc- multicellular glands. Nonsecretory áreas of the palate,
ture and function; also, the cloaca in caecilians is sexually buccal floor, and walls of the pharynx are lined with cil-
dimorphic in that a portion of the cloaca in males is iated epithelium.
eversible as a phallodeum. The structure and function of Multicellular buccal glands are present in most am-
 Integumentary, Sensory, and Visceral Systems
409

Figure 14-24. Semidiagrammatic

ventral views of the digestive organs
of amphibians. A. Salamander,
Necturus maculosus. B. Anuran,
Rana catesbeiana. C. Caecilian,
Siphonops annulatus. Abbreviations:
es = esophagus, gb = gall bladder,
li = large intestine, pa = páncreas,
si = small intestine, st = stomach.
The liver is shaded.

phibians, but they are absent in some aquatic taxa. Pre- like organs. Apically the receptor cells contain elabórate
sumably their absence in pipid frogs represents a loss of systems of intracellular membranes, and proximally the
this feature, whereas their absence in some oblígate neo- cells are in contact with afferent nene fibers.
tenic salamanders (Amphiuma, Siren) seems to represent The pharynx is an expanded chamber lined with cil-
arrested development; buccal glands are absent ¡n larval iated and mucus-secreting epithelium that lies posterior
salamanders. to the buccal cavity. A muscular sphincter sepárales the
The intermaxillary gland is formed of alveoli or tubules pharynx from the esophagus, and muscular actions open
within tíssues between (and also posterior to) the nasal and cióse the glottis, the entryway to the lungs.
capsules; the collecting ducts open to the anterior palatal
surface. In caecilians, the alveolar organs open sepa- Esophagus. The esophagus is a thin-walled tube ex-
rately, anterior and medial to the choanae. In salaman- tending from the pharynx to the stomach. It is a short
ders and anurans, the glandular región is more extensive, structure that is broad in cross section in anurans, some-
and in anurans it extends nearly to the córner of the what longer in salamanders, and long and slender in cae-
mouth. Furthermore, in anurans the secretory tubules cilians. At each end of the esophagus is a circular band
form a single glandular system secreting fluid from a com- of muscle that forms a sphincter. The lining of the esoph-
pact series of openings in the midline of the palatal sur- agus is in six to eight longitudinal folds. The mucosal
face. The secretion is sticky and when applied to the epithelium consists of cuboidal or columnar ciliated cells
tongue seems to serve in the entrapment of prey. (cilia absent in Proteus) with interspersed goblet cells; the
Choanal glands in the palatal epithelium empty into latter are most abundant anteriorly. Generally, four mus-
the choanae. The glands are large in anurans and some- cle layers are present. The innermost mucosal layer is
times nearly occlude the lumen of the choanal canal. The represented by minute bundles of longitudinal smooth
choanal glands of caecilians open at the margin of the muscle, but this is reduced in some salamanders (single
choanae, whereas those of salamanders open deep within fibers in proteids and essentíally absent in Tríturus). This
the choanae at the margin of the olfactory epithelium. layer and the adjacent submucosal layer become better
Two main kinds of taste buds (gustatory organs) are organized and developed near the stomach. The mus-
present in the buccal cavity in anurans (C. Jaeger and cular tunic is composed of a well-developed layer of cir-
D. Hulmán, 1976). These include papillary organs on the cular smooth muscle fibers. An outer layer of longitudinal
ápices of fungiform papillae on the dorsal surface of the fibers (when present) is sparse anteriorly and more robust
tongue and nonpapillary organs imbedded in the ciliated posteriorly.
epithelium throughout much of the buccal cavity and on Glands in the mucosal lining secrete mucus and pro-
the lateral surface of the tongue. Six types of cells in liferate pepsinogen. The glands of the latter type are con-
papillary organs are grouped into two classes— secretory centrated posteriorly and are absent in some salamanders
and receptor cells. The latter extend throughout the disc- (e.g., Salamandra) and anurans (e.g., Bambino and Pipa).
MORPHOLOGY
410 Stomach. The stomach usually lies to the left of the its immediate vicinity in Bufo and Hy/a, whereas the pan-
midline and is curved with the convex edge to the left. creatic duct joins the bile duct before the common duct
The stomach is broader, shorter, and more curved in leaves the páncreas in Rana.
anurans than in salamanders and caecilians. The mucosal
layer consists of unciliated epithelium with many slender, Digestive Process
spindle-shaped mucogenic cells, especially in the anterior The realization of nutrients is a suite of complicated
three-fourths of the organ. The muscular layers consist processes beginning with the capture of prey and ter-
of an inner, strong layer of circular muscle and a thinner, minating with the absorption of hydrolyzed components.
outer layer of longitudinal fibers. The posterior (pyloric) Prey capture and nutritíve valúes of prey are discussed
end of the stomach is separated from the duodenal por- in Chapter 9.
tíon of the small intestine by a distinct circular band of
muscles, the pyloric sphincter. Passage of Food. Movement of the food through the
digestive tract is by means of muscular and ciliary action.
Intestines. The intestine in amphibians is nearly uni- Food is forced from the mouth into the esophagus pri-
form in diameter throughout its length, except for a marily by the swallowing action of the tongue; small frag-
broader, straight portion posteriorly, the large intestine. ments are moved by action of buccal and pharyngeal
The intestine is nearly straight in caecilians, only slightly cilia. Food moves down the esophagus by peristaltic
folded in salamanders, and more elongate (proportion- muscular contractions. It is held in the esophagus until
ately) and folded in anurans. The muscular layers of both the muscles of the sphincter at the gastric end relax and
large and small intesünes are like those of the stomach. allow passage into the stomach, the anterior portion (fun-
The anterior portion of the small intestine, the duo- dus) of which is primarily a storage chamber. Slight mus-
denum, receives the bile and pancreaüc ducts. The mu- cle contractions in the wall of the stomach push the food
cosa of the intestine is folded in interspecifically different into the pyloric end of the stomach. Passage of food from
patterns, all of which greatly increase the surface área of the stomach into the duodenum is controlled by the small
the canal. Surface área is increased further by myriads intestine, where ¡ntermittent contractions of the muscular
of tíny projections, microvilli. The epithelial surface is wall move the contents posteriorly in the lumen. Strong
formed primarily by columnar cells interspersed with mu- contractions of the stomach and concomitant relaxatíon
coid goblet cells. Elabórate multicellular digestive glands of the sphincters at both ends of the esophagus permit
are unknown except in a few salamanders (e.g., Sala- regurgitation of the contents of the stomach. Mucus se-
mandra). creted by goblet cells in the pharynx, esophagus, and
The large intestine is separated from the small intestine small intestine lubricates the food, thus permitting ease
by a flaplike valve in some anurans; the valve is absent of passage through the alimentan; canal and preventing
in salamanders, caecilians, and primitive anurans. The mechanical damage to the lumen by sharp particles of
mucosal lining is composed of columnar epithelium in- chitin. Mucus secreted in the posterior part of the large
terspersed with goblet cells, which become more nu- intestine coats large concentraüons of the contents for
merous posteriorly. The terminal part of the tract is the defeca tion.
cloaca, which receives ducts from the reproductive sys-
tem and the urinary bladder. In salamanders in which Digestión. Ingested food is fragmented partially by the
fertilization is internal, the roof of the cloaca is modified teeth in most amphibians. Consequently, the exterior
into a spermatheca in females, and the walls contain surface, especially the chitin of insects, is subjected to
modified mucous glands in males (see Chapter 3). mechanical breakdown which allows the entry of diges-
tive enzymes into the soft tissues of the prey.
Associated Glands. Two glandular outgrowths of the Digestive enzymes generally are considered to be ab-
embryonic midgut are the liver and páncreas. The liver sent in the buccal secretions, but low concentrations of
is bilobate in anurans, elongate and sometimes emargi- diastatic amylase have been reported in the secretions of
nate in salamanders, and greatly elongate and slightly the intermaxillary, lingual, and pharyngeal glands in some
emarginate in caecilians. The gall bladder is attached to European species of Pelobates, Bufo, and Rana (Reeder.
the liver and empties into the duodenum via the bile duct. 1964).
The páncreas is enclosed in the hepato-gastric ligament Pepsinogen and mucus secreted in the esophagus ac-
and lies between the duodenum and the stomach. A crete around the food mass, but little or no mixture of
single pancreatic duct leads to the duodenum in anurans; secretions with the food takes place before the food reaches
2 or more ducts are present in caecilians and salamanders the stomach. The buccal and esophageal mucus, which
(up to 47 in Proteus). Differences exist in the mode of is alkaline, prohibits proteolytic digestión before gastric
entrance of the pancreatic duct to the duodenum in anu- acidification. Hydrochloric acid is secreted in the stom-
rans. Observations on European anurans by Dornesco et ach. The acidic storage chamber inhibits bacterial activity,
al. (1965) showed that the duct opens to the bile duct in hastens the death of still-living prey, and begins the de-
the wall of the intestine in Bombina and Pelobates or in calcification of bone. In the low pH of the pyloris, pep-
 Integumentary, Sensory, and Visceral Systems
sinogen is transformed to pepsin, which attacks proteins. dian pars intermedia and pars distalis, and the bilateral 411
Digestión is completad in the small intestine, in which pars tuberalis, which is absent in some salamanders.
the contente of the lumen are mixed with a variety of Bilateral hypothalamo-hypophyseal neurosecretory fi-
digestive enzymes by intermittent contractions of the ber tracts extend posteriorly from the paired preoptic nu-
muscular wall. Mucoid secretions in the duodenum neu- clei in the ventral wall of the hypothalamus. Some of
tralize the acidic material received from the stomach. these tracts termínate in the median eminence and others
Erepsin secreted by glands in the small intestine hydro- extend to the pars nervosa; some fibers termínate in the
lyzes peptones and proteases to amino acids. Secretin pars intermedia in Trituras cristatus and in some species
from the duodenal mucosa sümulates the reléase of pan- of Rana. Blood is supplied to the neurohypophysis by
creatic juices. the hypophyseal artery, and hypophyseal portal vessels
Bile salte from the gall bladder break down fats. Other extend from the median eminence into the pars distalis.
digestive enzymes in the small intestine are secreted by The functional capacity of the entire pituitary is de-
the páncreas. Of these, trypsin hydrolyzes protein; am- pendent on its nervous and vascular association with the
ylase is active in the hydrolysis of glycogen and starches hypothalamus. These connections are responsible for the
to simple sugars; and Upase facilitates hydrolysis of fats control of pituitary secretions in response to both exterior
and glycerides to fatty acids and glycerol. No amphibians and endogenous stimuli integrated in the brain. The ad-
are known to possess enzymes that facilítate the break- enohypophysis is under neurosecretory regulation man-
down of keratin, chitin, or cellulose. ifested by means of nerve fibers of the hypothalamo-
hypophyseal tract or the hypophyseal portal vessels. The
Absorption. Absorption commences in the small in- pituitary is an essential link in the neuroendocrine system,
testine, where nutriente are absorbed by the extensive even though all of its secretions are controlled directly or
capillary system in the walls of the intestine. Absorption indirectly by the brain.
of water and salte takes place in the large intestine. The pars distalis produces five hormones. Two gonad-
otropic hormones (follicle-stimulating hormone and lu-
teinizing hormone) are released cyclically in response to
ENDOCRINE GLANDS exterior stimuli mediated in the brain. Their effects on
The regulation and coordination of various organs is the gonads and the feedback mechanism are discussed
manifested either by electrochemical impulses transmit- in Chapter 2. Prolactin has a variety of effects (Bern and
ted by nervous tissue or by complex chemical substances, Nicoll, 1969): (1) sümulation of the water-drive and in-
hormones, carried by the vascular system. Hormones are tegumentary changes in efts of Notophthalmus virídes-
produced by the endocrine glands. Amphibians have all cens, (2) secretion of oviducal jelly, (3) proliferation of
of the endocrine glands that are known in other tetra- melanophores, and (4) stimulation of larval growth (see
pods, and with few exceptions it seems that the endocrine Chapter 7). Thyrotropin srimulates the secretion of thy-
secretions of amphibians resemble those of other verte- roxin, and adrenocorticotropin acts on the cortical cells
brales. of the adrenal glands to promote the output of adrenal
In this section the structure and function of the endo- steroids.
crine glands are described, and the sources and actions The pars intermedia secretes melanophore-stimulatíng
of their producís are discussed. A summary of the en- hormone (intermedin, MSH) which affects integumentary
docrine glands and their products in amphibians is by chromatophores; MSH causes dispersal of melanosomes
Gorbman (1964). Much information on amphibians is in melanophores and pigmentary organelles in xantho-
included in texts on endocrinology, especially by C. Tumer phores, and causes the aggregation of reflecting platelets
and Bagnara (1976), and a recent thorough account of in iridophores.
the hormonal control of amphibian metamorphosis is Neurohypophyseal hormones from the pars nervosa
provided by A. White and Nicoll (1981). The hormones are importan! in regulating water loss and salt balance
produced by endocrine glands, their targets, and their (see Chapter 8). Antidiuretic hormone (ADH) primarily
actions are summarized in Table 14-2. causes an increase in the rate of reabsorpüon in the tu-
bules of the kidney; secondarily it causes a decrease in
Pituitary the rate of glomerular filtration. Arginine vasotocin and
The pituitary is closely associated with the ventral surface the less effective oxytocin act on the skin and membranes
of the diencephalon. It develops from a unión of the distal of the urinary bladder and kidney tubules to increase
end of a saclike diverticulum from the floor of the dien- passive permeability to water, salte, and urea and to stim-
cephalon called the infundibulum and a solid ectodermal ulate active transport of sodium.
dorsal protrusion from the buccal cavity. The infundibular
part of the gland, the neurohypophysis, consiste of two Thyroid
regions, the pars nervosa and the median eminence (Fig. The thyroid glands are paired structures in the throat.
14-25). The part derived from the buccal protuberance, The glands develop as a median growth from the ventral
the adenohypophysis, consiste of three regions—the me- wall of the pharynx and then sepárate and move pos-
MORPHOLOGY
412 Table 14-2. Endocrine Glands, Their Hormones, Target Áreas, and Actions

Gland/hormone Target área Action

Pituitary: pars distalis
Follicle-stimulating hormone Germinal epithelium Stímulates maturation of
(FSH) ovarían follicles
Luteinizing hormone (LH) Testícular interstitial tíssue Stímulates production of
testosterone
Prolactin Lower oviducts Production of oviducal jelly
Integument Glandular changes
Integument Proliferatíon of melanosomes
Caudal and gilí tissues Growth
Thyrotropin (thyroid- Thyroid Stímulates thyroid secretíons
stimulating hormone,
TSH)
Adrenocortícotropin (ACTH) Adrenal cortex Promotes output of adrenal
steroids
Pituitary: pars intermedia
Melanophore-stimulating Integument Color change
hormone (MSH)
Pituitary: pars nervosa
Antídiuretic hormone (ADH) Kidneys Concentratíon of uriñe
Arginine vasotocin Skin, kidneys, urinary bladder Increases permeability to water
and salts
Oxytocin Skin, kidneys, urinary bladder Increases permeability to water
and salts
Thyroid
Thyroid hormones Various tissues Metamorphosis (see Table 7-2)
Parathyroids
Calcitonin Bones and kidneys Metabolism of bone and
minerals
Parathyroid hormone (PTH) Bones and kidneys Metabolism of bone and
minerals
Ultímobranchial bodies
Calcitonin Bones and kidneys Metabolism of bone and
minerals
Thymus
Thymosin Lymphopoietíc sites Stímulates production of
lymphocytes
Pineal body
Melatonin Integument Aggregatíon of melanosomes
Pancreatic islets
Insulin Liver, muscles, adipose tíssue Facilitates assimilation of sugar
Adrenal: medulla
Adrenalin Cardiovascular system Increases heart rate;
vasodilatíon
Skeletal muscle Increases blood flow
Liver and brain Increases blood flow
Kidneys Decreases blood flow
Noradrenalin Cardiovascular system Increases heart rate;
vasoconstriction
Kidneys Decreases blood flow
Adrenal: interrenal
Cortícosteroids Intestine and skeletal muscles Metamorphosis
Gonads: testes
Testosterone Germinal epithelium Promotes spermatogenesis
Integument Development of secondary sex
characteristícs
Gonads: ovaries
Estrogen Germinal epithelium Formation of primary follicles
Progesterone Ovarían follicle cells Initíates maturation of
postvitellogenic ova

terolaterally to a point on the dorsal surface of the the hypoglossal (C.N. XII). The glands are supplied by
m. sternohyoideus in anurans. The glands are situated the thyroid branch of the external carotid artery and
more laterally in salamanders and caecilians. Accessory drained by the thyroid vein which carnes blood to the
thyroid follicles occur in the throat musculature. Each external jugular vein.
gland consists of a series of closed follicles innervated by The thyroid hormones, tetraiodothyronine (thyroxin.
 Integumentary, Sensory, and Visceral Systems
hypophyseal artery- adults and lie next to the larynx in anurans (absent in 413
Xenopus) and caecilians. Only the gland on the left side
persists in most salamanders, but in oblígate neotenes
such as Amphiuma and Necturus the glands are paired.
The ulümobranchial bodies produce calcitonin (or a cal-
citonin-like substance) which affects metabolism of min-
erals. These glands are especially active during meta-
morphosis (see Chapter 7).

Thymus
.oothalamo-
The thymus gland originales as several paired thickenings
•. oophyseal
tract—' on the dorsal side of the pharyngeal pouches. The first
-median hypophyseal six pouches produce thymus buds in caecilians; the first
eminence portal vessels and sixth buds are lost, and the others fuse into a single
; ; ure 14-25. Diagrammatic sagittal section of the hypophyseal
gland on each side. In salamanders the buds are asso-
región of a frog, Rana temporaria, showing the relative positions of ciated with the first five pouches, but the first two are
ÍK components of the pituitary gland and the associated lost; this results in a trilobate gland on each side. In some
seurosecretory tracts. The parts of the pituitary are: PD = pars
Sstalis, PI = pars intermedia, PN = pars nervosa. Adapted from anurans, buds origínate only from the first and second
Dierickx and van den Abeele (1959). pouches, and the first is lost (Noble, 1931b). In all adult
amphibians the glands are located beneath the skin on
either side of the throat. Secretions of the thymus gland,
T¿) and triiodothyronine (T3), have profound effects on collecüvely known as thymosin, play major roles in im-
morphological and functional changes during metamor- munity by stimulating lymphopoiesis (E. Cooper, 1976).
phosis (see Chapter 9). Thyroid hormones in postmeta-
morphic amphibians have been implicated in (1) oxida- Pineal Body
ive and other metabolism, (2) integumentary structure, The pineal body is a median outgrowth of the thalamus
and (3) nervous function. However, the experimental re- on the dorsal surface of the brain. This structure is sen-
sulte in all of these áreas are ¡nconclusive (Gorbman, sitive to light, and prolonged darkness stimulates the re-
1964). léase of melatonin, a hormone which aggregates mela-
nosomes in melanophores in the skin, thereby resultíng
Parathyroids in a lightening of the color of the skin. Melatonin also
The parathyroids are small, spherical, encapsulated glands may promote the reléase of prolactin by the pars distalis
closely associated with the external jugular veins. The two of the pituitary during larval development (Gutiérrez et
pairs of glands arise from ventral growths of the third and al., 1984).
fourth pharyngeal pouches. Parathyroids are absent in at
least some oblígate neotenic salamanders (e.g., Necturus Pancreatic Islets
maculosus). The activity of the glands seems to be sea- In addition to secreting digesrive enzymes, the páncreas
sonal at least in températe species of anurans, in which contains masses of cells referred to as the Islets of Lan-
the glands degenerate in winter. gerhans. These glands develop from pancreatíc ducts in
The parathyroids secrete calcitonin and parathyroid larvae and become functional at metamorphosis. The is-
hormone (PTH); both hormones are important in cal- lets secrete insulin which is transported by the hepatíc
cium metabolism (Bentley, 1984). Many species of am- portal vein. Insulin is essential for carbohydrate metabo-
phibians seem to utilize PTH as a hypercalcemic hor- lism by facilitating the assimilation of sugar by tissues.
mone; the calcium stores in the bones and paravertebral
''lime sacs" apparently are the primary sites for the effects Adrenals
of this hormone. Furthermore, PTH promotes the acti- The adrenal glands are composed of tissues of sepárate
vaüon of vitamin D3 to 1,25-dihydroxycholecaliferol, which origins. Chromaffin cells are neuroectodermal, and the
also has a hypercalcemic effect resultíng in increased ab- cortical (= steroidogenic) and Stilling cells are meso-
sorptíon of calcium from the intestine and renal glomer- dermal. The chromaffin cells consütute the medullary part
ular filtrate and enhanced resorpüon of calcium from bone. of the gland, whereas the cortical and Stilling cells form
On the other hand, calcitonin has a hypocalcemic effect the interrenal portion; the latter is considered to be a
on body fluids because it is antagonistic to the resorpüve sepárate gland by some workers. The function of Stilling
process from bone and possibly enhances excretion of cells is unknown. The adrenals are elongate structures
calcium in the uriñe. on the ventromesial surface of each kidney in caecilians
and salamanders. They are proportionately shorter struc-
Ultimobranchial Bodies tures on the midventral surface of each kidney in most
These small glands origínate as epithelial growths from anurans; are ventromesial in leiopelmatids, discoglossids,
the sixth pharyngeal pouch. The glands are paired in and pipids; medial in Pelobates; and lateral to the mid-
MORPHOLOGY
414 section of the kidney in more advanced anurans (Grassi act in concert to provide an effective means of cutaneous
Milano and Accordi, 1983). respiration. The various combinations of branchial, pul-
Two catecholamines are secreted by the chromaffin monary, and cutaneous respiratíon are unique to am-
cells in the adrenal medulla. The principal hormone is phibians.
adrenalin (= epinephrine) which chiefly affects the car- The integumentary stucture of amphibians is related
diovascular system and blood flow through the brain, not only to respiration but also to water balance. The rich
liver, kidneys, and skeletal muscle (Table 14-2), as well supply of cutaneous capillaries is important in water and
as increases the rate of metabolism of blood sugars. The ion diffusion as well as gas exchange; these subjects are
second hormone, noradrenalin (= norepinephrine), discussed at length in Chapter 8. The integument also
funcüons in much the same way as adrenalin, but the contains the poison glands; these reléase combinations
effects of the latter usually are much stronger than that of toxins that are unique to amphibians and that are
of noradrenalin. The two hormones are antagonists in important in protection from predators (see Chapter 10).
the vascular system in that adrenalin is a vasodilatator, The eyes of amphibians represen! the first evolutionary
whereas noradrenalin generally is a vasoconstrictor. Ad- step in vertébrate terrestrial visión, with powers of ac-
renalin also can cause melanosome aggregatíon in integ- commodation and generally with eyelids and associated
umentary melanophores and increases in the activity of glands and ducts. Depth perceptíon and true color visión
integumentary glands in anurans. are present. Green rods in the retina are unique to am-
Adrenal cortical (= interrenal) secretíons that have been phibians and allbw them to perceive a diverse range of
identífied are steroids—aldosterone, corticosterone, and wavelengths.
cortísol; the circulating levéis of these hormones change The auditory apparatus is uniquely amphibian, espe-
during metamorphosis, and they have been implicated cially with the presence of papilla amphibiorum and a
in morphological changes occurring at metamorphosis columellar-opercular complex, which, depending on the
(see Chapter 7). degree of modificatíon of the component systems, allows
The activity of the adrenal glands is controlled primarily for the effective receptíon or airborne and/or seismic sig-
by levéis of the pituitary hormone adrenocorticotropin náis.
(ACTH) in the blood; ACTH stimulates adrenal activity. Although the class Amphibia is characterized by a suite
of features of the internal anatomy, each of the three
Gonads living orders has certain characters that are different from
The development and structure of the gonads have been the others. Salamanders are the most generalized, whereas
described in the foregoing section: Urogenital System. anurans seem to have numerous derived characters.
Although the gonads are primarily reproductive organs, Caecilians have many specializations associated with their
they produce and secrete hormones that are importan! attenuate body form (e.g., reduced left lung, asymmetri-
in the endogenous control of reproductive cycles and the cal reduction of aortic arches) and fossorial existence (e.g.,
development of secondary sex characters. The endocrine sensory tentacle, reduced eyes).
activity of the gonads is controlled by the pituitary go- It is tempting to utilize some of the features of the
nadotropins. Luteinizing hormone influences the produc- intemal systems in phylogenetíc reconstruction. For ex-
tíon of the male androgen, testosterone, in the interstitial ample, caecilians, salamanders, and leiopelmatid frogs
cells of the testes. Testosterone facilitates spermato- share the apparently primitive states of a simple patch of
genesis and promotes the development of secondary sex papilla amphibiorum and kinocilia of the auditory epi-
characters such as nuptial excrescences (see Chapter 3). thelium lacking terminal bulbs, whereas other anurans
The ovarían follicles produce estrogen which promotes have an elongate patch of papilla amphibiorum and bulbed
the proliferation of the germinal epithelium in the ovary kinocilia. Likewise, the position of the adrenal gland in
and the formatíon of primary follicles, but the maturation the presumed primitive families of anurans (leiopelma-
of the follicles depends on follicle-stimulating hormone tíds, discoglossids, pipids) is like that of salamanders and
from the pituitary. In at least one species, the viviparous caecilians on the ventromesial side of the kidney, whereas
anuran Nectophrynoides occidentalis, progesterone is se- in more advanced anurans the position of the gland is
creted by the corpora lútea (see Chapter 2). shifted laterally.
A major problem exists in the use of many of these
features of soft anatomy in drawing phylogenetic conclu-
EVOLUTIONARY CONSIDERATIONS sions. In contrast to osteológica! characters, the details of
It is commonly stated that amphibians are morpholog- the internal organ systems are known for very few taxa,
ically intermedíate between fishes and amniotes. This is and there is virtually no knowledge of the intraspecific
generally true for the gross morphology of the nervous, variation. Much more descriptive work needs to be done
digestíve, and urogenital systems. However, other sys- on many more taxa before characters of the internal sys-
tems are specialized and have characters that are unique tems can be employed with confidence in evolutionary
to the amphibians. This is partícularly true of the integ- studies.
ument and the circulatory and respiratory systems which
 PART

EVOLUTIOJV
 CHAPTER 15
But the great gulfwithin the vertébrala lies
between Físhes andAmphibia... . On the
side ofthe fishes onfy the Dipnoi and the
Crossopterygii come into consideration.
Hans Gadow (1901)
Origin
and Early
Evolution

H Lumans, throughout recorded history, have at-

tempted to explain the phenomena of nature that sur-
Osteichthyes, a group that appeared in marine waters
and that, by the Devonian, inhabited marine and fresh-
round them. The study of evolutionary biology is merely water environments as well. Included in this class are
the disciplined pursuit of the same end—a methodology three major groups of fishes—Actínopterygii (ray-finned
by which scientists seek to explain the existence of or- fishes), Dipnoi (lungfishes), and lobe-finned crossopter-
ganisms and the processes by which organisms change ygian fishes (Actinistia of some authors). From the actín-
through time. Thus, it is entirely understandable that ver- opterygians aróse the multitude of bony fishes that dom-
tébrate biologists in general, and amphibian biologists in inate marine and freshwater habitáis today. This group
particular, long have been preoccupied with the question is distinguished from both dipnoans and crossopterygians
of the origin of the most primitive tetrapods, the am- by its possession of (1) short-based, paired fins and (2)
phibians. Many theories have been advanced and count- ganoid scales. In contrast to the actinopterygians, the dip-
less scenarios constructed to account for the appearance noans and crossopterygians are characterized by (1) paired
of the first amphibians in the Upper Devonian and the fins having a pronounced, fleshy, lobed base that con-
subsequent evolution of the group. The theories and the tains robust skeletal elements, and (2) cosmoid scales.
scenarios, like the organisms, have evolved as more and The cosmoid scale is formed from thickened dermal bone
more evidence has accumulated and as we have become composed of several layers—a lowermost, lamellar, bony
more perceptive in our understanding of the mechanisms layer, overlain by a highly canaliculate vascular layer, a
of evolutionary change. The discussion that follows is a typical dentine layer with a peculiar "pore-canal" system
synthesis of our progress to date. Those who seek res- (dentine + pore-canal system + enamel = "cosmine"),
olute solutions and incontrovertible fact may be dissat- and a thin superficial cover of enamel-like material. Gan-
isfied, but hopefully the imagination of the perceptive oid scales differ in their lack of a pore-canal system and
reader will be challenged by the nature of the evidence in their possession of múltiple layers of enamel (= "gan-
and the conflicting emphases and interpretations of it that oine").
have led to substantially different views of the origin of The characters that distínguish dipnoans and crossop-
amphibians. terygians from other bony fishes also ally them with the
All evolutionary biologists concede that the ancestor to primitive tetrapods. The question of which of the two
amphibians is to be found among bony fishes of the class groups is related most closely to the tetrapods is equiv-

417
EVOLUTION
418 oca\an¿ likely will remain so for years to come, as will with, or intimately united to, the posterior oüco-occipital
become evident in the discussions that follow. part of the braincase (Fig. 15-1).
2. Posterior (otico-occipital) región of skull longi-
tudinally compací.—Clearly, this is a relative character,
NATURE OF A TETRAPOD but in contrast to crossopterygians and some dipnoans,
In seeking the origin of the tetrapods, we first must define the posterior región of the braincase (i.e., that part pos-
them. Is the group monophyletic (i.e., including the most terior to the orbit) of tetrapods is relatívely short com-
recent common ancestor and all of its descendants) or pared with the facial región (Fig. 15-1; see Gaffney, 1979,
not? Although this question has been subject to consid- for review of literature).
erable controversy during this century (see D. Rosen et 3. Jugular vein and truncus hyoideo-mandibularís
al., 1981, for review), the majority of scientists today of facial nerve (CJV. VII) pass across dorsal surface
agree that the Tetrápoda represent a natural, monophy- of hyomandibular bone and orbital artery runs through
letic assemblage that is defined by a suite of characters hyomandibular bone.—Classically, the possession of a
described by Gaffney (1979) (for an alternaüve view- bone lying between the auditory capsule and the cheek
point, see Jarvik, 1980-81). Thus, all tetrapods, both or otic región has been interpreted to be a middle-ear
fossil and Recent, are presumed to possess the characters bone, i.e., the stapes or columella, that functionally is
described below, although some of these characters may part of the impedance- matching system involved in sound
have been modified or lost secondarily in derived taxa. transmission; as such, a middle-ear bone was thought to
1. Salid braincase.—The braincase is that part of the be a universal character of tetrapods (Gaffney, 1979).
skull that endoses the brain exclusive of those parts that However, Carroll (1980) suggested that in the Lower
house the sense organs (e.g., nasal and auditory cap- Carboniferous labyrinthodont amphibian Greererpeton
sules), and the dermal covering bones. The braincase is this bone braced the cheek región against the braincase,
derived embryologically from the chondrocranium, a car- thereby providing interna! cranial support as the skull
tilaginous endoskeleton that is formed by developmental became freely movable on the trunk and a more solid
fusíons of sepárate cartilage components (see Chapter attachment between the dermatocranium and braincase
6). In tetrapods, the anterior (ethmosphenoid or eth- evolved. Thus, the long-accepted distinction between the
moidal + orbitotemporal) portion of the braincase is fused hyomandibular bone of fishes as a suspensory element
and its homologue in tetrapods, the middle-ear bone
(stapes or columella), as a sound-transmittíng element is
no longer appropriate. Smithson and Thomson (1982)
reported that in the osteolepiform fish Eusthenopteron
ethmoidal orbitotemporal foordi the hyomandibular bone articulates with two dis-
crete facéis (the lateral commissure) that protrude from
the lateral aspect of the auditory capsule. The jugular
canal lies between these two facéis and serves as the
entrance into the head for the orbital (= stapedial) artery
and the exit from the head of the jugular vein and truncus
hyoideo-mandibularis of the facial nerve. From the jug-
LN.
ular canal, the nerve passes through the hyomandibula
LN.IX
N. I-1 LN. IV fenestrá ovajis
via the hyomandibular canal. In contrast, in early tetra-
N.V&VII pods the lateral commissure and jugular canal are absent,
N.h and the truncus hyoideo-mandibularis does not pass
through the "hyomandibula." Instead, this nerve, along
with the jugular vein, passes across the dorsal surface of
the hyomandibula and the orbital artery runs through the
hyomandibula. Apparently, this is a primitive arrange-
'-•-"« «v**^-*— •sf—~^>v^mr
x t*F
ment for all tetrapods and represents a fundamental dis-
tinction between fishes and amphibians. However, the
ethmoidal orbitotemporal occipital arrangement is independen! of any shift between sus-
pensory and auditory functions. Following Smithson and
Figure 15-1. A. Braincase in lateral view of Eusthenopteron foordi Thomson (1982), the terms "stapes" and "columella"
(about x 1), an osteolepiform fish, redrawn from Jarvik (1980-81). are associated here with the condition characterisüc of
B. Eogyrínus attheyi (about x 3), a labyrinthodont amphibian, tetrapods, in which the canal for the truncus hyoideo-
redrawn from Panchen (1972). Note the presence of the
intracranial joint (indicated by arrow) in Eusthenopteron and the mandibularis has been lost and a new canal has devel-
differences in regional proportions of the skulls of these oped for the orbital ( = stapedial) artery.
representatives of crossopterygians and primitive amphibians,
respectively. The locations of major cranial nerve foramina are 4. Presence of an otic notch.—The endoskeleton of
shown for each braincase. the skull, the chondrocranium, is invested superficially by
 Origin and Early Evolution
membrane bones that compose the dermatocranium. dermal elements, together with the elaboration of the 419
Topographically, these are arranged into the following scapulocoracoid, is associated with the modification of
regions: (1) snout anterior to orbits, (2) margins of orbits, the pectoral skeleton for terrestrial locomotion by means
3) skull table covering the braincase and temporal fossae of fore- and hindlimbs in primitive tetrapods (Fig. 15-5).
that house jaw-closing muscles, (4) cheeks that form the 9. Well-developed pelvis with iliac blades that ex-
lateral walls of the temporal fossae, and (5) marginal tooth- tend dorsally to articúlate uiith an ossified sacra! ríb
bearing bones. The otic notch is a dorsolateral, V-shaped (ríbs) of the vertebral column.—The possession of limbs
cleft in the skull roof; the notch is formed between the for terrestrial locomotion presupposes a structural link by
posterodorsal edge of the cheek and the posterolateral which the support provided by the hindlimbs is trans-
edge of the skull table (Figs. 15-2A, 15-2B, 15-17-19). mitted to the body (Fig. 15-5). The tetrapod pelvis is
The notch is presumed to have been present in all prim- composed of three endochondral elements on each side—
itive amphibians except the lepospondyls, in which it is the ilium, ischium, and pubis—which together form a
assumed to have been lost. Superficially, the otic notches cup-shaped depression, the acetabulum, that provides
of all amphibians and reptiles appear to be similar, and for the articulation of the head of the fémur. The pu-
at one time they were assumed to be homologous struc- boischiac píate surrounding the acetabulum provides a
tures that housed the eardrum or tympanum. In some surface for muscle attachment. The robust median unión
primitive amphibians (e.g., Greererpeton), however, it of the two halves of the girdle, together with the iliac
has been found that the stapes attached distally to the blades that articúlate with the vertebral column, assures
cheek región; thus, it is questionable whether in these that support from the hindlimbs is transmitted to the body.
animáis the otic notch actually housed an eardrum and 10. Well-developed, ventrally oriented ríbs.—The
therefore whether their so-called otic notch is homolo- possession of well-developed presacral ribs is associated
gous with those of other primitive amphibians (e.g., tem- with an elaboration of axial musculature and support of
nospondyls) and the reptiles. For the time being, the the body cavity (Fig. 15-5).
presence of an otic notch is accepted conditionally as a
tetrapod feature with the realization that future findings
may reveal that this character is not homologous in those PRIMITIVE TETRAPODS
animáis in which it occurs. An understanding of the evolution of early tetrapods in
5. Single pair of nasal bones with or without a sin- general, and early amphibians in particular, necessitates
gle median ossification (internasal).—Nasals are der- a knowledge of certain fossil amphibians.
mal investing bones that roof the olfactory región on either
side of the midline (Figs. 15-2A, 15-6A, 15-19A, and 15- Labyrinthodont Amphibians
20A). The nasals may be separated by a median ossifi- The most primitive tetrapods known are the labyrintho-
cation; occasionally they are fused or entirely lost, but dont amphibians, which are known from Upper Devon-
they never are replaced by múltiple, median ossifications ian to Triassic fossils. Although these organisms represent
(Figs. 15-10-12). a diverse morphological assemblage, they share the suite
6. Fenestra ovalis.—The stapes (= columella) com- of characters listed above that are unique to tetrapods.
municates with the cavum labyrinthicum of the inner ear Based on the fossil record, we are able to describe gen-
vía the fenestra ovalis, or oval window, an opening in erally the basic structure of these ancient organisms—a
the lateral wall of the auditory capsule (Fig. 15-21). step that is critica! not only to our appreciation of the
7. Carpuá, tarsus, and dactyly.—Tetrapods bear fore- morphological changes that occurred as animáis became
and hindlimbs with wrist and ankle joints, respectively, better adapted to a terrestrial mode of existence, but to
and digits on the manus and pes. Furthermore, it has our understanding of the relationships among them, and
been suggested that the possession of four digits on the between them and the crossopterygian and dipnoan fishes.
manus and five digits on the pes is the primitive condition
for tetrapods and that the prepollex (= precarpale fide Skull. The skulls of labyrinthodont amphibians are
Schaeffer, 1941) and postminimus (= postcarpale) do massive and completely roofed by dermal investing bones
not represent the remains of additional digits (see Gaff- (Figs. 15-2, 15-6A, 15-6C, 15-17A, and 15-17B). The
ney, 1979, for review of arguments). snout (i.e., preorbital portion of the skull) tends to be
8. Pectoral skeleton free from skull; posttemporal, long, whereas the otico-occipital portion is relatively short.
supracleithrum, gilí cover, and anocleithrum absent; The composition of the dermatocranium is relatively fixed.
scapulocoracoid relatively larger than dermal shoul- Thus, the skull roof is composed of nasals, frontals, and
der elements.—The posttemporal, supracleithrum, and parietals. The upper jaw is made up of premaxillae and
anocleithrum are dorsodistal dermal bones of the pec- maxillae, both of which bear sharp, cone-shaped, laby-
toral girdle of crossopterygian fishes (Fig. 15-14). Be- rinthine teeth. The maxillary arch is united to the sus-
cause the posttemporal and gilí cover ( = operculum) pensorium by the quadratojugal. The orbit is enclosed
unite the girdle to the skull, their loss marks the inde- by a circle of bones—prefrontal, postfrontal, jugal, and
pendence of these two units. The loss of all of these lacrimal. The temporal fossa, which accommodates the
EVOLUTION
420 B
sensory canal quadratojugal-]
prefrontal
premaxillary
nasal
lacrimal
maxillary
snout—
orbit frontal
jugal postfrontal
parietal -
intertemporal vomer

supratemporal

-otic notch
|ectopterygoid
-quadrate
occipital condyle-1 Habular
postparietal
jugal
pterygoid

Figure 15-2. Skutl of Palaeoherpeton decorum,

a labyrinthodont amphibian (about x Vs),
redrawn from Panchen (1970). A. Dorsal view. quadratojugal
B. Lateral view. C. Posterior view. D. Ventral pterygoid •foramen magnum parasphenoid—' Lopísthotic
view. For details of labyrinthodont teeth, see
Figure 15-13. basioccipital—'

jaw musculature, is roofed by one or two bones, the

supratemporal and intertemporal; frequently, either one
or both of these elements are absent. Laterally, the squa-
mosal, quadratojugal, and part of the jugal endose the
temporal fossa, thereby forming a "cheek región." Be-
cause both the squamosal and quadratojugal articúlate
with the quadrate, they also are part of the suspensory
apparatus. The posterior margin of the skull roof is bor-
dered variably by a series of supraoccipital elements—
the postparietals medially and the tabuláis laterally. There
is a single external narial opening, the external naris on
each side of the skull; the naris usually is bordered by
the premaxilla, maxilla, nasal, and lacrimal, and/or sep-
tomaxilla, if the latter is present.
An extensive palate is formed by dermal bones, many
of which bear large teeth (Figs. 15-2D, 15-6B, 15-17B,
and 15-17D). The vomers floor the nasal capsules an-
teriorly and form the anteromedial margin of each mem-
ber of the single pair of internal narial openings, or
choanae. The pterygoids lie posterior to the vomers and presplenial
lateral to the braincase; they not only form a substanüal
part of the palate, but also brace the quadrate and maxilla -postsplenial
against the central auditory and neurocranial regions of L surangular

the skull. A pair of bracing elements parallel the maxilla

Figure 15-3. Jaw of labyrinthodont amphibian, Eogyrinus atthe.vi
and lie between this bone and the pterygoid and/or vomer. ( x Vs), redrawn from Panchen (1970). A. Lateral view. B. Lingual
The most anterior of these, the palatine, forms the pos- or medial view.
 Origin and Early Evolution
tenor or posterolateral border of the choana. Posteriorly, structure characteristic of labyrinthodonts (and all tetra- 421
the ectopterygoid articulates with the maxilla laterally and pods except some amphibians) is the apsidospondylus,
the pterygoid medially or posteromedially. The vomer, or "arch vertebra," in which the centrum región of each
palatine, and ectopterygoid usually bear teeth. A median, vertebra is composed of two sets of ossifications—the
longitudinal dermal invesüng bone, the parasphenoid, anteroventral intercentra and the posterodorsal pleuro-
floors the braincase posterior to the vomers and between centra. The lepospondylus, or "husk vertebra," charac-
the pterygoids. terizes small Paleozoic and some advanced amphibians
The fused braincase interna! to the dermatocranium (i.e., salamanders and caecilians), but the homology of
(Fig. 15-1B) is composed of several ossifications that are these vertebrae is suspect in view of the many vertebral
identifiable primarily by their general location owing to modifications observed among Paleozoic amphibians. The
fusión of the elements in adults. The anterior braincase centrum of a lepospondylous vertebra is a single, spool-
is formed by the sphenethmoid. Posteriorly, the opis- shaped structure that primitively was pierced by a length-
thotic and prootic endose the auditory región. The back wise hole that accommodated the persistent notochord
of the braincase is composed primitively of up to four (Fig. 15-4D).
sepárate elements—the ventromedial basioccipital, dor- There are several subtypes of arch vertebrae. In the
somedial supraoccipital, and paired exoccipitals. The rhachitomous type (Fig. 15-4A), the intercentrum is me-
basioccipital bears rounded, knoblike structures, occipital dian, ventral, wedge-shaped in lateral view, and crescent-
condyles, by which the skull articulates with the first, or shaped when viewed end-on. The pleurocentra are much
cervical, vertebra. smaller, paired blocks that are located dorsally between
The lower jaw of primitive amphibians is complex by successive neural arches and intercentra. Depending on
comparison with more recent forms, being composed of the relative contribution of the intercentrum and pleu-
as many as 10 elements (Figs. 15-3, 15-6D, and 15-6E). rocentrum to the development of the centrum, several
The primary tooth-bearing element of the mandible is other types of arch vertebrae can be distínguished. In the
the dentary. Laterally, this bone is supported by a series stereospondy/ous condition (Fig. 15-4B), the pleurocen-
of four dermal bones; in an anterior to posterior sequence trum is absent or reduced to such a point that the cen-
these are the splenial, postsplenial, angular, and suran- trum is formed entirely by the paired intercentra that grow
gular ( = infradentaries 1-4 of Jarvik, 1980-81, and other upward to form complete, or nearly complete, rings around
works). Lingually, the dentary is supported by as many the notochord. If both the intercentra and pleurocentra
as three coronoid bones, which also bear teeth. The pos- contribute to the centrum, the vertebra is called embol-
terior portion of the mandible is composed of a large
preartícular and a relatively smaller articular that articu-
lates with the quadrate.
Little is known about the visceral skeleton of primitive
amphibians, because these elements rarely were pre-
served as fossils. However, one component can be iden-
tified—the stapes or columella. Where preserved, this
element extends from the auditory capsule to the cheek
región or dorsolaterally from the auditory capsule to the
región of the otic notch.

Axial Skeleton. The axial skeleton of primitive am-

phibians is well developed in order to support the weight
of the body in terrestrial environments. The vertebral col-
umn, per se, is composed of a series of well-ossified ver-
tebrae, each of which bears a neural arch enclosing the
spinal cord dorsally and anterior and posterior processes,
zygapophyses, that provide for articulation between ad-
jacent vertebrae (Figs. 15-4 and 15-5). Ribs are associ-
ated with vertebrae between the neck and the proximal
part of the tail. Anterior ribs are bicapitate, whereas more
posterior ones are unicapitate. In the región of the pelvic
girdle, the ribs are modified; these sacral ribs articúlate
with the iliac blades of the pelvic girdle.
Two disünct types of vertebrae characterize primitive Figure 15-4. Two successive vertebrae of labyrinthodont
amphibians. The difference involves the structure of the amphibians in left lateral view. A. Rhachitomous, Eryops.
B. Stereospondylus. Mastodonsaums. C. Embolomerous,
vertebral centrum, the cylindrical body of the vertebra Eogyrinus. D. Lepospondylus, Pantylus. A-C redrawn from
that surrounds and replaces the notochord. The centrum Panchen (1980); D from Panchen (1977).
EVOLUTION
422

Figure 15-5. Restoration of Icthyostega sp. in lateral aspect from Jarvik (1980-81). Total length of
specimen about 65 centimeters. Note massive pectoral girdle that is independent of the skull, broad ribs, and
fusión of most posterior vertebrae into a rod. The dorsomedial tail fin supported by endoskeletal elements
and dermal fin rays is atypical of other primitive tetrapods. Reproduced with permission of Academic Press.

omerous (Fig. 15-4C). In an alternative arrangement hindlimb. Midventrally, the paired pubes and ischia form
characteristic of one of the major groups of labyrintho- a broad píate. The upper part of the pelvic girdle is com-
donts, the anthracosaurs, the intercentra are reduced, posed of dorsal or posterodorsally directed ilial blades
and the paired pleurocentra grow downward to form a that articúlate with the sacral ribs.
ring around the notochord.
Limbs. The basic structure of the fore- and hindlimbs
Pectoral Girdle. The primitive amphibian shoulder is quite similar. Robust proximal elements, the humerus
girdle is a robust structure that is independent of the skull and fémur, articúlate with the pectoral and pelvic girdles,
and capable of supportíng the anterior half of the body respectively (Fig. 15-5). Distally each of these elements
by providing expansive surfaces for the origin of massive articúlales with paired longbones—the radius and ulna
muscles used to move the head and forelimbs (Figs. 15- of forelimb, and tibia and fíbula of hind limb. In each
5 and 15-7). The ventral portion of the girdle consists of case, the inner bone of the pair (i.e., the radius and tibia,
two, fíat, chest plates. The smaller anterior píate is formed respectively) tends to rest directly under the proximal
by a single, median, longitudinally oriented interclavicle limb bone and, therefore, supports much of the weight
flanked on either side by the clavicles, whereas the pos- of the body. Muscles pulling on the outer, or lateral, bone
terior píate is composed of large paired coracoids. Dorso- of each pair, the ulna and fíbula, tend to extend the distal
laterally the plates articúlate with the upper part of the fore- and hindlimbs, respectively. The wrist and ankle are
pectoral girdle, the scapular píate, which incorporates the composed of a complex of small elements, the carpus of
cleithrum along its leading edge. At the junction of the the forelimb and the tarsus of the hindlimb. Typically,
upper and lower portíons of the girdle, an articular sur- the elements are arranged such that there is a proximal
face is formed for the humerus, the proximal bone of the row of three or four relatively large elements lying be-
forelimb. tween the lower limb bones and the remaining, smaller
carpa! or tarsal elements. The remaining elements can
Pelvic Girdle. The pelvic girdle is a massive structure be divided into two groups. There is a series of four or
providing for muscle attachments from the hindlimbs, and five distal carpáis and five tarsals, each of which is as-
connecting the hindlimbs to the vertebral column via the sociated with the proximal head of a digit. The inner three
sacrum (Figs. 15-5 and 15-8). The unión of three bones distal carpal and tarsal elements (associated with Digits
on each side (pubis anteriorly, ischium posteriorly, and I-HI) articúlate proximally with three small elements known
ilium dorsally) forms the acetabulum—the articular sur- as the centralia.
face for the head of the fémur, the proximal bone of the The articulation of these short, robust limbs with mas-
 Origin and Early Evolution
sive girdles allows for anterior-posterior-ventral limb ro- Ichthyostega: The Earliest 423
tation. The structure of the limbs is such that there are Known Tetrapod
two points of flexión—proximally at the elbow and knee, ¡chthyostega is one of three genera of primitive amphib-
and distally at the wrist and ankle. Thus, the stocky, low- ians that have been discovered from the Upper Devenían
slung primitive amphibians probably were capable of lift- of eastern Greenland. Of the two other genera, Ichthy-
ing their bodies off the ground. ostegopsis is placed in the same family as Ichthyostega

internasal palatal fenestra B

•premaxillary premaxillary
nasal external
W/XLWI i ftii inaris
i%ii i «a
septomaxillary
lateral rostral
vomer
mternal naris
/•™«¡—lacrimal
^—prefrontal
palatine
pterygoíd /Osff !•?/,'•. „','///,
.maxillary l*&\\\\^!li/l'
parasphenoid
ectopterygoid
parietal

supratemporal

quadratojugal-

*.***jr
L-tabular notochordal canal —
-preopercular supraorbital—i r-postorbital

otic notch

sensory canal subopercular

r-prearticular
articular fossa
coronoid 1
infradentary 4

infradentary 3—' —anterior coronoid

Figure 15-6. Skull and mandible of Ichthyostega sp. (about x Vi), redrawn from Jarvik (1980-81). A. Skull
in dorsal view, B. ventral view, and C. lateral view. D. Mandible in lateral view and E. lingual view. Note
the remnant of a preoperculum (A), presence of a suboperculum (C), position of external nares (B, C), and
incorporaron of notochordal canal into posterior portion of braincase (B). Compare with Figure 15-2.
Nomenclature of elements of lower jaw follows Jarvik (1980-81); thus, infradentaries 1-4 are equivalen! to
the presplenial, postsplenial, angular, and surangular, respectively, as illustrated in Figure 15-3.
EVOLUTION
424 (Ichthyostegidae), and Acanthostega in a sepárate family is supported by endoskeletal elements (radiáis) and der-
(Acanthostegidae). This material is represented only by mal fin rays (lepidotrichia) characteristic of fishes (Fig. 15-
partíal skull tables, whcreas complete skulls and post- 5). The most posterior vertebrae are fused into a bony
cranial elements are assignable to ¡chthyostega (Fig. 15- rod. The individual vertebrae are rhachitomous (Fig. 15-
5). Thus, the following discussion centers on features of 4A), and each presacral vertebra supports a pair of bi-
the best-known fossil material. capitate ribs. The ribs are unusual in that each is com-
The discovcry of ¡chthyostega had profound effects on posed of an anterior, curved rodlike portion, from which
our characterization of tetrapods and descriptíon of their a posterior laminar píate arises. Successive ribs overlap
probable origins. Because Ichthyostega was stratigraph- one another to form a rigid armor that endoses the body
ically older and anatomically more primitíve than its Car- cavity. The ribs diminish in length posteriorly. The con-
boniferous relatives, it was anticipated that this organism ditíon of the sacral rib(s) is unknown; however, a few
would prove to be morphologically intermediate between posterolaterally oriented postsacral ribs have been de-
the Carboniferous labyrinthodonts and the rhipidistian, scribed.
lobe-finned fishes, which at that time were accepted al-
most universally as the closest relatives of primitive tetra- Pectoral Girdle. Although the general architecture of
pods. The position of ¡chthyostega as the most primitive the pectoral girdle is similar to that of other labyrintho-
tetrapod is unassailable at present, but unfortunately, the donts, there are significant differences in the components
animal did not conform to the preconceived model. For of the girdle. The upper portion is represented by a
example, many features of the skull are primitive relative bladelike structure, the cleithrum (Fig. 15-7); the distinct
to those of other labyrinthodonts, but at the same time scapular píate of other labyrinthodonts is absent. More-
there are significant differences in proporüons between over, the coracoid píate bears a posterior depression and
the skull of Ichthyostega and those of osteolepiform fishes. supraglenoid process atypical of other primitive tetra-
Moreover, many structures are still unknown in Ichthy- pods.
ostega (e.g., the soft anatomy, structure of the manus,
braincase, and detailed dispositíon of the sensory cañáis). Pelvic Girdle. The pelvic girdle of ¡chthyostega (Fig.
It is the existence of apparently discordant characters and 15-8A, 15-8B) is represented by a single ossification, in
the lack of information about others that has prompted contrast to the three, paired bones characteristic of other
some recent authors (e.g., D. Rosen et al., 1981) to rein- tetrapods. Despite this, distinct pubic, ischial, and ilial
terpret morphological trends and reassess the phyloge- portions of the girdle can be ¡dentified, and the overall
netíc relationships of primitive tetrapods. In view of the structural plan is nearly idéntica! to that of other labyrin-
importance of ¡chthyostega, a resume of its characters is thodonts.
presented below. Unless specifically stated otherwise, it
can be assumed that the foregoing, generalized descrip- Limbs. The forelimb of Ichthyostega is known only
tion of primitive tetrapods also applies to Ichthyostega. from the próxima! limb bones. The bones of the wrist are
too disarticulated to be described, and the digits are un-
known. The radius and ulna resemble the corresponding
Skull. The snout of ¡chthyostega is similar in general
elements of other labyrinthodonts; however, the humer-
aspect to that of other primitive amphibians (Fig. 15-6).
us is distinctive. In contrast to the robust bone of other
The external nares are not visible in dorsal view because
labyrinthodonts, the main distal part of the humerus of
they are located low on the lateral margin of the maxillary
Ichthyostega has three thin blades oriented in medial,
arch, as they are in some Lower Carboniferous labyrin-
lateral, and dorsal planes.
thodonts. The same bones participate in forming the The hindlimb is shorter and stockier than that of other
margin of the nares, with the exceptíon of the maxilla.
primitive amphibians (Fig. 15-7C). In particular, the tibia
The posteroventral margin of the naris is constituted by
and fíbula are short, broad elements that articúlate me-
a slip of bone that has been interpreted as a slender
dially throughout their lengths. The tarsus is composed
process of the maxilla or a sepárate bone, the lateral
of a broad but short tibíale, fibulare, and ¡ntermedium
rostral. In addition to the usual dermatocranial elements,
that articúlate distally with 11 compact tarsal elements.
Ichthyostega has a remnant of a preoperculum applied
The five digits are exceedingly short and stubby.
to the posterior margins of the squamosal and quadra-
tojugal and a suboperculum that lies posteriorly adjacent
to, but sepárate from, the quadratojugal. In contrast to
all other primitive amphibians, a large notochordal canal TETRAPOD AFFINITIES:
is incorporated into the posterior braincase. With the ex- LUNGFISHES OR LOBE-FINS?
ceptíon of the jaws, the visceral skeleton of Ichthyostega At the time of this writing, there are two schools of thought
is unknown. regarding the closest relatives of fossil and Recent tetra-
pods. The debate is largely methodological—an expres-
sion of what is generally conceded to be the neontolog-
Axial Skeleton. ¡chthyostega is distinguished from other ical viewpoint versus the paleontological. The paleontol-
labyrinthodonts in possessing a dorsomedial tail fin that ogist seeks to demónstrate changes in anatomical reía-
 Origin and Early Evolution
425

cleithrum

supraglenoid
subscapular foramen
fossa supraglenoid
process

glenoid
fossa

supracoracoid
glenoid canal— coracoid píate foramen

interclavicle

clavicle
coracoid píate

subscapular fossa

cleithrum

Figure 15-7. Pectoral girdle of

¡chthyostega sp. A. Endoskeletal
girdle and cleithrum of right half of
girdle in medial view. B. Right side
in lateral view. C. Restoration of
entire girdle in dorsal view. Note the
bladelike cleithrum and supraglenoid
process atyical of other primitive
tetrapods. Redrawn from Jarvik
(1980-81).

üonships in the fossil record—a data matrix that is re- of thought attempt to construct evolutionary trees (i.e.,
stricted by the fragmentary nature of most fossils, gaps branching diagrams) based on nested sets of derived fea-
in the fossil record, and a lack of knowledge of soft an- tures, most neontologists do not seek to identify specific
atomical features. Neontologists, on the other hand, seek ancestors of Recent taxa or to define ancestor-descend-
to demónstrate evolutíonary changes by comparative ant sequences. As a consequence of this methodological
morphological studies of extant species, deriving the evo- dichotomy, some biologists claim that lungfishes and te-
lutionary change ¡n characters by comparisons with closely trapods share a common ancestor that is not shared by
related forms not included in the group under study. Fur- any other groups, and therefore are related more closely
thermore, neontologists seek to define homologies on the to one another than either is to any other group (Fig. 15-
basis of ontogeneüc changes of characters in the species 9A). Those biologists who base their arguments only on
under study; they also include features of soft anatomy, features preserved in the fossil record favor a scheme in
development, and physiology in their argument. Most which the osteólepiform lobe-fin fishes (of which Eusth-
paleontologists look for ancestors—an ancestor-descend- enopteron foordi is the best-known representativa) are
ant sequence in which ancestors are assumed to be more related most closely to primitive tetrapods (Fig. 15-9B).
generalized in a particular character, and the descendants Evidence for both views is summarized below.
more specialized. Whereas proponents of both schools Dipnoans are known from marine habitáis in the Early
EVOLUTION
426 articular área
for sacral rib
iliac portion

iliac canal

acetabulum
pubic portion

I— ischiatic portion obturator cañáis

postminimus
fibulare
IV

Figure 15-8. Pelvic girdle and

hindlimb of Ichthyostega sp.
A. Right side of pelvic bone in lateral
view. B. Right side of pelvis in
medial view. C. Left hindlimb in
externa! view. Note that pelvis is tibia
composed of a single ossification intermedium
rather than three sepárate bones as
in other primitive tetrapods. Redrawn tibíale prehallux
from Jarvik (1980-81). tarsal I tarsale prehallucus

Devonian. Although these specialized forms are moder- Comparativa Morphology

ately abundant and diverse in the fossil record, they are
represented by only five species in three genera today— Skull. In general proporüons, the skulls of many dip-
Neoceratodus (Australian lungfish), Protopterus (African noans and all osteolepiforms are markedly different from
lungfish), and Lepidosiren of South America. Lungfishes those of primitive tetrapods in that the postorbital (i.e.,
are elongate, round in cross section, and bear two pairs otico-occipital) length is much shorter in tetrapods (com-
of lateral fins that are long, slim, fleshy structures with pare Figs. 15-2, 15-10, and 15-11). Both dipnoans and
slightly webbed margins in Protopterus and Lepidosiren, osteolepiforms are characterized by a complex mosaic of
but broader, fleshier structures in Neoceratodus. External dermal bones dorsally that bear questionable homologies
nostrils are absent, but there are two pairs of narial open- to the relatively fixed pattern observed in primitive tetra-
ings (excurrent and incurrent) associated with the inside pods, owing to the application of different criteria of ho-
of the mouth. A spiracle is absent. Both lungs and gills mology (for a review of the arguments, see D. Rosen et
are present. al., 1981). Neither group has a pair of bones that can be
Osteolepiform crossopterygians are also known from designated as nasals; instead the snouts of each group
marine and freshwater habitats of the Devonian and Car- are covered by an irregular mosaic of small bones. The
boniferous, but they became extinct in the early Permian. posterior skull table (Fig. 15-12) is a special source of
The osteolepiforms bore two pairs of lateral fins which, debate. If skull bones are defined relative to their position
in contrast to those of dipnoans, were short with a more with respect to the eyes, then ichthyostegids are more
robust, fleshy base. Only one pair of narial openings similar to dipnoans than to osteolepiforms. On the other
pierced the palate, and one pair of external nares was hand, if we assume (1) that the eyes and pineal foramen
present on the dorsal aspect of the snout. A spiracle, are capable of shifting their positions, but (2) that the
lungs, and gills supposedly were present. lateral line cañáis occupy the same positions in the cranial
 Origin and Early Evolution
-Osteichthyes -Osteichthyes , 437
Actmopterygü Sarcopterygii ( Sarcopterygii-
Actmopteri- -Choanata- -Choanata —

B
Figure 15-9. Character-state trees for major groups of 38. Reduction or loss of hypobranchials.
Osteichthyes, after A. Rosen et al. (1981) and B. Schultze (1981). 39. Reduction or loss of pharyngobranchials.
Broken lines indícate an unresolved cladistic position. Numbered 40. Inferior vena cava present.
characters refer to shared, derived features (synapomorphies). For 41. Pulmonary vein present.
cladogram A, the characters are: 42. Choana present.
8. Dermal skull bones with internal processes attaching to 43. Labial cavity present.
endocranium and various toothed dermal bones on palate. 44. Second metapterygial segment of paired appendages
9. Endochondral bone. composed of paired subequal elements that are functionally joined
10. Lepidotrichia and ceratotrichia in fins. distally.
11. Radiáis of fins never extending to fin margin. 45. Two primary joints in each paired appendage, between
12. Two or fewer preaxial radiáis associated with first two endoskeletal girdle and unpaired basal element and between basa)
metapterygial segments of pectoral fin endoskeleton. element and paired elements of second segment (in pectoral
13. Dermal sclerotic ring of four plates. appendage, preaxial member of paired elements with ball-and-
14. Marginal upper and lower jaw teeth on dermal bones lateral socket joint with basal and postaxial member articulating on
to palatoquadrate. dorsal—postaxial—margin of basal element).
15. Interhyal (= stylohyal) present. 46. Reduction of ratio of dermal fin rays to endoskeletal supports
16. Infrapharyngobranchials with forward orientation. in paired appendages.
17. Suprapharyngobranchials present on first two gilí arches. 47. Tetrapodous locomotion in living representatives.
18. Gilí arches 1 and 2 articulating on the same basibranchial. 48. Muscíes in paired fins segmented.
19. A pneumatic or buoyancy organ as an outpocketing of the 49. Fusión of right and left pelvic girdles to form pubic and
anterior gut (lung, swimbladder). ischial processes.
20. Absence of supramaxillary (jugal) canal joining infraorbital 50. Hyomandibula not involved in jaw suspensión.
canal. 51. Loss in interhyal ( = stylohyal).
21. Differentiated propterygium in pectoral fin. 52. Hyomandibula reduced and, at least in extant forms, joined
22. Modification of pelvic fin metapterygium to form parí or all dorsally by ligament and closely associated with otic recess in the
of pelvic girdle, and endoskeletal support of pelvic fin exclusively by braincase, and ventrally with quadrate.
preaxial pelvic radiáis. 53. Loss of dorsal gilí arch elements (pharyngobranchials).
23. Acrodin caps on all teeth. 54. Opercular bone, in extant forms, reduced and joined
24. An exclusively metapterygial pectoral and pelvic fin posteriorly by a división of the epaxial musculature to the upper
supported by a single basal element, and an anocleithrum in the half of the primary shoulder girdle.
shoulder girdle suspensión. 55. Right and left pterygoids joined in midline, excluding the
25. Absence of the connection between the preopercular and parasphenoid anteriorly from the roof of the mouth.
supratemporal lateral-line canal. 56. Loss of autopalatine.
26. Enamel on teeth. 57. Elongation of snout región.
27. Sclerotic ring of more than four plates. 58. Eye somewhat posterior in skull, at about level of junction
28. Anocleithrum of dermal shoulder girdle sunken beneath between two principal bones in skull roof.
dermis and lacking surface ornamentation. 59. Pattern of five dermal bones covering otic and occipital
29. Clavicle large relative to cleithrum, and pectoral appendage regions of braincase.
insertion high as compared with those conditions in 60. Resorption of calcified cartílago and subsequent deposition of
actinopterygians, cladistians, and Eusthenopteron. bony tissue in vertebrae of Devonian Gríphognathus (lungfish) is
30. Both pectoral and pelvic appendages with long, muscular idéntica! with the formation of bony tissue in uncalcífied cartilage
lobes that extend well below body wall and with structurally similar ¡n Tetrápoda.
endoskeletal supports. 61. Numerous features of soft anatomy, development, and
31. Preaxial side of pectoral fin endoskeleton rotated to postaxial physiology.
position. For cladogram B, the characteristics are:
32. A series of canal-bearing bones (for supraorbital canal) la. Teeth composed of true enamel.
lateral to large, paired, roofing bones between orbits. Id. Plicident teeth.
33. Absence of hyostyly in jaw suspensión. 3a. Prearticular present ín lower jaw.
34. Posterior margin of palatoquadrate erect or sloping backward 3d. Three coronoid bones in lower jaw.
rather than sharply forward from jaw articulation. 5. One pair of choanae in roof of mouth.
35. Presence of a rostral organ. 8. Endoskeleton of paired fins lacking in archipterygium.
36. Basibranchial, single, broad, and triangular. Discussion of these characters may be found in Rosen et al.
37. Last gilí arch articulating with base of preceding arch rather (1981) and Schultze (1981).
than with basibranchial.
EVOLUTION
428
notch for
mcurrent nostril

\e tooth

"pterygoid

,quadrate

parasphenoid

V
Figure 15-10. Skull and mandible
of Devenían lungh'sh, Dípteras
valenciennesi. A. Dorsal view of
dermatocranium. B. Restoration of
palate. C. Dorsal view of mandible. symphysial mandibular
D. Lateral view of mandible. Note píate tooth píate
irregular mosaic of small bones that
composes skull roof (position of eyes
is hatched), presence of crushing
tooth ptates instead of plicident
teeth, position of both excurrent and
incurren! narial openings in roof of oral canal bones-
mouth, and relatively long otico-
occipital portion of skull. The upper
jaw lacks marginal bones (maxilla
and premaxilla) typical of
osteolepiforms and tetrapods. A and
B redrawn from Jarvik (1980-81); C
and D from Jarvik (1967).

bones of fishes and amphibians, then the posterior skull and primiüve amphibians seem to resemble one another
table of osteolepiforms is more similar to that of amphib- more closely than either group resembles lungfishes.
ians than that of dipnoans. Dipnoans are unique in that there are no narial open-
Both fossil and Recent lungfishes are disünct from os- ings on the exterior of the skull. Rather, the incurrent
teolepiforms and ichthyostegids in their lack of the typical opening lies on the lingual margin of the jaw and the
marginal jaw bones—i.e., maxillae and premaxillae excurrent opening in the roof of the mouth (Fig. 15-10B).
(compare Figs. 15-6, 15-10, 15-11), and possession of This condition contrasts with that characterizing osteole-
crushing toothplates (Fig. 15-10) instead of cone-shaped piforms and tetrapods in which there is an external naris
teeth composed of folded dentine, or plicidentine (Fig. (incurrent opening) on the snout and an infernal palatal
15-13). Dipnoans are highly specialized in their posses- opening, the choana (Fig. 15-1 IB). The quesüon of the
sion of a toothed, bony preoral eminence instead of pre- homology of the dipnoan excurrent opening and the
maxillae, and lateral nasal toothplates instead of maxillae. choanae of osteolepiforms and tetrapods is debated (see
Miles (1977) suggested that the preoral eminence and D. Rosen etal., 1981; Miles, 1977; and Jarvik, 1980-81,
nasal toothplates were derived from the premaxillae and for reviews). In some actinopterygian fishes, there is a
maxillae of gnathostome fishes. However, the histology third opening in the palate región that looks similar to a
of the preoral eminence and the toothplates is quite dis- choana. In these fishes, as well as dipnoans, there is no
tinct from that of the premaxillae (Miles, 1977) and pli- evidence that the nasal apparatus ever transmits air into
cident teeth (Schultze, 1970) of osteolepiforms and prim- the buccal cavity, as ¡t does in tetrapods; instead it is
itíve amphibians. Thus in these respects, the osteolepiforms purely an olfactory mechanism. The tetrapod choana de-
 Origin and Early Evolution
- nasorostropremaxillary 429
vomer

fenestra
exochoanalis
dermatopala-
tine

ectoptery-
goid

sphenoid

entopterygoíd

supratemporal

Figure 15-11. Skull and mandible

of an osteolepiform fish,
Eusthenopteron foordi, redrawn from
Jarvik (1980-81). A. Dorsal view of
dermatocranium. Note mosaic of
small bones ¡n nasal área, dorsal
position of external nares, position of
pineal foramen between eyes (which
are hatched), and relative length of
otico-occipital portion of skull.
Sensory cañáis indicated by broken
lines. B. Ventral view of skull. Note
interna! choanae, presente of
marginal jaw bones (maxillae and
premaxillae), and presence of true
teeth. C. Lateral view of mandible.
D. Medial view of mandible. The
endocranium of Eusthenopteron is
L-prearticular shown in Figure 15-1 A. Terminology
-mandibular symphysis follows Jarvik (1980-81).

velops embryologically from the unión of an interna! those of lungfishes (Fig. 15-10B—D) are reduced. The
process of the nasal sac and a small diverticulum from palates of some dipnoans lack both the palatine and ec-
the gut—a morphogenetic process not observed in lung- topterygoid, and the lower jaw is composed of only six
fishes. In the absence of information on the ontogeny of elementa of disputed homologies (see Miles, 1977, for
the choana in osteolepiforms, we can never be certain review). Among fossil dipnoans showing less reductíon
that this structure is homologous to that of tetrapods; than Recent species, the lingual side of the mandible is
however, its location in the palate and relationship with composed of a large prearticular and a small, median
the external naris on the snout suggest that it is homol- adsymphysial píate. In lateral aspect there is a short, an-
ogous (but see D. Rosen et al., 1981, for a difieren! terior dentary and a canal-bearing infradentary series
view). consisüng of a variety of bones of unknown homologies.
The palate and mandible of osteolepiforms (Fig. 15- Dipnoans apparently lack the coronoid bones and artic-
11B-D) largely correspond to those of tetrapods, whereas ular characteristic of osteolepiforms and primitive tetra-
EVOLUTION
430

Figure 15-12. Comparison of skull tables (stippled bones) of A. an osteolepid fish, Panderichthys, B. a
lungfish, Griphognathus. and C. a labyrinthodont amphibian, Ichthyostega. Pineal foramen (A, C) shown in
black. Sensory cañáis indicated by broken lines and orbits by cross-hatching.

pods, and the mandible is equipped with crushing tooth-

plates or denudes rather than teeth.
The endocrania or braincases of both lungfishes and
tetrapods are considered to be fused in contras! to those
of osteolepiforms, which are divided into an anterior eth-
mosphenoid portion and a posterior otíco-occipital por-
tion (Fig. 15-1). Dorsally, the dermal roofing bones form
a transverso suture that coincides with the marginal abut-
ment of the two halves of the braincase (Figs. 15-11A
and 15-12A). The conditíon in osteolepiforms has been
termed a hinged braincase. The so-called fused endo- D
crania of lungfishes and tetrapods seem to be of two
distinct types. In nearly all tetrapods the braincase is at
least partially ossified; there is a single pair of anterior
ossifications in the ethmosphenoid portion of the endo-
cranium, whereas múltiple centers of ossification com-
pose the oüco-occipital part of the braincase. In all tetra-
pods, except Ichthyostega, the anterior and posterior
ossifications of the neurocranium are bridged dorsally by
dermal roofing bones. In general, post-Devonian dip-
noans have poorly ossified crania, with ossification being
restricted to the occipital región and partial dermal ossi- Figure 15-13. Maxillary teeth in lateral view of three
fication of the walls of the cranial cavity (Miles, 1977). labyrinthodont amphibians. A. Lanceolate teeth of Anthracosaurus
russelli (natural size) and B. Eogyrínus attheyi (natural size)
The heavy and complete ossification of the endocraniurn compared to chisel-shaped teeth of C. Archeria crassidisca ( x 2).
of Devonian forms offers no clue to regional centers from Note prominent longitudinal ridges. D. Transverse section of
which ossification proceeded. Based on the available evi- palatine tusk of Eogyrinus attheyi at alveolar level, showing
characteristic infolding of dentine ( x 4). Redrawn from Panchen
dence, the endocrania of osteolepiforms and tetrapods (1970).
seem to be more nearly comparable than those of dip-
noans and tetrapods.
chordal sheath may have been invaded by sclerotomal
Axial Skeleton. The vertebral skeleton of lungfishes cells to produce amphicoelous vertebral centra (with or
is strikingly different from that of osteolepiforms. Among without a notochordal canal) upon which cartilaginous
some fossil dipnoans, there is evidence that the noto- neural and hemal (i.e., arcualia) arches rested. In some
 Origin and Early Evolution
other fossils, the arcualia ossified. Recent lungfishes retain and tetrapod shoulder girdles. Lungfishes and osteole- 431
sepárate, cartilaginous arcualia around the notochord; piforms are similar in sharing a connection of the dermal
cartilaginous vertebral bodies are found only in the tail. pectoral skeleton to the posterior margin of the skull. In
The single set of unicapitate pleural ribs is ventral—i.e., Eusthenopteron (Fig. 15-14), the dermal pectoral skele-
they are formed along the line of contact of the lining of ton consists of six elements; in a dorsal-ventral sequence
the body cavity (somatopleure) with the myoseptum, in these are: posttemporal, supracleithrum, anocleithrum,
contrast to the dorsal rib of tetrapods that forms along cleithrum, clavicle, and interclavicle. The posttemporal
the intersection of the horizontal septum and myosep- and supracleithrum bear the sensory canal connecting
tum. the lateral line of the body with the temporal canal of the
In contrast, the vertebrae of osteolepiform fishes are head. The postcleithrum articúlales with the temporal re-
composed of ossified arcualia that nearly surround the gión of the skull and the cleithrum ventrally. The clavicles
notochord in a rhachitomous fashion. The intercentra form and interclavicle form an anteromedian breastplate. Little
the major part of the centrum with small posterodorsal is known about the endoskeletal components, but it is
components; it is uncertain whether the latter represent suspected that there existed a dorsal scapular extensión
paired pleurocentra or nonhomologous, intercalary ele- and an anteroventral and medial clavicular portíon
ments. The neural arch is well developed and ossified, (= scapulocoracoid?), and a tuberosity providing an ar-
but lacks the zygapophyses with adjacent neural arches ticular surface for the pectoral fin.
that characterize tetrapods (Fig. 15-4). The ribs of Eus- Lungfish pectoral girdles are best known in Recent taxa,
thenopteron are short, unicapitate, and dorsal. and these are characterized by a reduced number of der-
mal components (Fig. 15-15A-C). The anocleithrum is
Pectoral Girdle. A great deal remains to be learned the most dorsal element. It is reduced in size, is bifúrcate,
about the homologies of the elements of the pisciform and lies within the epaxial musculature and within a liga-

endoskeletal
shoulder girdle
glenoid process
humerus
entepicondylar ulna
process
ulnare

intermedium ray
supracoracoid foramen radius i-rprepollex
subscapular fossa
interclavicle
clavicle

cleithrum

endoskeletal shoulder girdle

pisiforme

Figure 15-14. Ventral parís of exo- and endoskeletal shoulder girdle and endoskeleton of pectoral fin of the
osteolepiform flsh Eusthenopteron foordi. A. Right side, medial view. B. Right side, lateral view. C. Both
halves, dorsal view. Redrawn from Jarvik (1980-81).
EVOLUTION
432
~ iA anocleithrum

endoskeletal
shoulder girdle

humerus—'
Figure 15-15. Appendicular
elements of a lungfish, Neoceratodus i—ulna & radius
forsterí. A. Endo- and exoskeletal
components of pectoral girdle in left
lateral, B. left medial, and fémur -tibia & fibula
C. complete dorsal views.
D. Endoskeleton of left pectoral fin
and E. pelvic fin in position of rest
against body. A—C redrawn from
Jarvik (1980-81); D-E redrawn from
Rosen et al. (1981).

ment joining the posterior margin of the cranium to the by a pair of small scapulocoracoids that are joined mid-
girdle in Protopterus (Jollie, 1962), but is larger and not ventrally and that bear a lateral tuberosity, against which
bifúrcate in Neoceratodus (D. Rosen etal., 1981). Cleith- the proximal bone of the pectoral fin articúlales. Accord-
rum-clavicle relatíonships are not clear. According to Jol- ing to Jollie (1962), the scapulocoracoid articúlales with,
lie (1962), the cleithrum is much reduced and the clavicle and is partly supported by, a massive "rib" attached to
extends from near the dorsal edge of the cleithrum and the occipital región of the head—an observation not dis-
closely approaches the midline. In contrast, D. Rosen et cussed by D. Rosen et al. (1981).
al. (1981) claimed that the clavicle was not reduced in The variation observed in osteolepiform pectoral gir-
Neoceratodus and (based on Schmalhausen's, 1917, work) dles, together with the conflicting and unresolved inter-
reported that the clavicle and cleithrum of Protopterus pretations of the dipnoan girdle, suggests that much more
are fused to form a single element. needs to be known about this character complex to ren-
The endochondral skeleton of lungfish is represented der it really useful in assessing phylogenetic relationships.
 Origin and Early Evolution
Pclvic Girdle. Unlike those of primitive tetrapods, the dipnoans and osteolepiforms are as different from one 433
pelvic girdles of dipnoans and osteolepiforms are de- another as each is from those of primitive tetrapods.
pressed, lacking a prominent dorsal iliac process. The two
halves of the girdle are fused in lungfishes, whereas there Limbs. The limbs of osteolepiforms and dipnoans are
is a median articulation in Eusthenopteron. Both bear strikingly different (compare Figs. 15-14, 15-15D, 15-
prominent anterior pubic processes; in dipnoans the ele- 15E, and 15-16), but presumably both types of limbs
ments are long, slender, median, and fused throughout evolved from the same primitive, finned ancestor. Two
their lengths, whereas in Eusthenopteron the robust ele- theories have been postulated to explain the mechanism
ments are oriented anteromedially and articúlate at their by which discrete fins evolved; there is no conclusive
anterior ends. The ilium of Eusthenopteron, together with evidence to support one over the other. According to the
the presumed posteromedial ischial región, forms a pos- fin-fold theory, the ancestral vertébrate possessed a pair
terolaterally oriented articular surface for the fémur; the of continuous ventrolateral fin folds from which the paired
ischium bears a posteromedially oriented ischiadic process. fins aróse by selective persistence of certain áreas of the
In contras! to Eusthenopteron and tetrapods, which bear fin fold and eliminaüon of others. The body-spine theory
a dorsal iliac process, the pelvic girdle of dipnoans is a holds that early fishes possessed ventrolateral spines and
long, slim, anterolaterally oriented structure. A postero- that fins developed, first, as a flap of skin that extended
lateral articular surface for the proximal fin element seems from the spine to the body wall; subsequently the spine
to be formed in the posterior ischium-ilia región, and was elaborated into an endoskeletal framework support-
each ischium bears short, slender posterior processes that ing the fin. Regardless of the origin of the fins and their
are fused ventromedially. Clearly the pelvic girdles of support, it is postulated that the endoskeleton might have

fíbula—i
fémur—, postmínimus
fibulare

intermedium—
l_ prehallux

pubic portion

pelvic bone

iliac portion
obturator groove

fémur

tibia

ischiatic portion
postminimus
Figure 15-16. Restoration of the pelvic girdle
and endoskeleton of the pelvic fins of the
osteolepiform fish Eusthenopteron foordi.
A. Lateral view. B. Dorsal view. Redrawn from
Jarvik (1980-81).
EVOLUTION
434 consisted of a preaxial (i.e., leading-edge) spine with a in the amount of nuclear DNA within the neotenic fam-
posterior, longitudinal series of basal piales (pterygio- ilies of salamanders or between salamanders and dip-
phores); fin rays (dermatotrichia) may have extended lat- noans. Instead, there is a cióse relatíonship between in-
erally from the pterygiophores into the membranous fin. creased amounts of nuclear DNA and larger cell size in
Loss of the preaxial spine and differentiation of the basal both groups (Thomson, 1972; Morescalchi, 1975). Szar-
plates may have resulted in a fin composed of series of ski (1970) suggested that nuclear hypertrophy and as-
three large, longitudinally oriented basal plates associated sociated low rates of cellular metabolism were physiolog-
with lateral rods (radiáis). The typical ray-fin of actino- ical adaptations to stagnating aquatic habitáis.
pterygians can be derived from this prototype through a There are at least two significan! features in which Re-
constriction of the fin base by reduction in size of the cent amphibians and lungfishes differ. (1) All Recent am-
basáis and loss of some basáis and most radiáis. In the phibians and amniotes (with the possible exception of
primitive lobed or biserial fin, the basáis form a longitu- some marine hydrophiid snakes) possess Bowman's glands
dinal axis from which lateral rods radíate; short fin rays in the olfactory epithelium. These glands are absent in
extend from the radiáis to the edge of the fin. Lungfishes all fish, including the dipnoans (Parsons, 1959). (2) In
retain the primitive biserial fin (Figs. 15-15D, 15-15E), amphibians, the testís is connected with some of the an-
whereas osteolepiforms have a more derived limb, in terior kidney tubules, and the entire Wolffian duct ¡s used
which the longitudinal basal axis of the fin has shifted to for sperm transport; there is a strong tendency for the
the posterior, postaxial border of the fin and the radiáis formaüon of accessory urinary ducts from the posterior
extend toward the preaxial and distal borders (Figs. 15- part of the kidney. The reverse pattern characterizes
14, 15-16). The resulting limb is short, stout, and com- lungfishes, in which the entire Wolffian duct is used for
posed of a single proximal bone that articúlales distally uriñe transport, and the testis is connected to the pos-
with a pair of robust elements. The latter, in turn, artic- terior end of the kidney, much as it is in actinopterygian
úlate with a series of asymmetrically arranged elements fishes (Gerard, 1954; Parsons and E. Williams, 1963).
that have been homologized with carpal and tarsal ele-
ments of tetrapods (Jarvik, 1980-81; D. Rosen et al., Discussion
1981). The origin of primitive amphibians from crossopterygian
ancestors is entrenched firmly in the literature of the past
Other Characters 50 years. Untíl recently, few have quesüoned seriously
Some of the most persuasive arguments applied by those the premise that the closest relatives of primitive tetra-
who seek to ally dipnoans and amphibians involve soft pods were to be found among the osteolepiform fishes.
anatomical features, development, and physiology, the But controversies have emerged ¡n the face of changing
nature of which are unknown in fossil forms. These char- methodologies involved in solving phylogenetic problems
acteristics are discussed at some length by Schmalhausen and the accumulation of more and diverse data. In as-
(1968). For the purposes of this discussion it should be sessing the relative merits of the two different phyloge-
pointed out that Recent amphibians and lungfishes share netic schemes presented above (Fig. 15-9), it is importan:
the following characters: (1) lungs that are structurally to note that two fundamentally different approaches have
similar internally and that are supplied with blood from been involved. Thus, D. Rosen et al. (1931) and Gar-
the last pair of aortic arches; (2) a circulatory pattern in diner (1982, 1983) in seeking to determine the closest
which blood is returned from the lungs via the pulmonary relatives of the tetrapods, have ¡dentified patterns of
vein and the left side of the sinus venosus to the left part morphological change by means of study of ontogeny
of the atrium; (3) presence of an elongate valve in the and comparative anatomy—clearly an approach that must
conus arteriosus that partially sepárales arterial and ve- rely primarily on data gathered from extant organisms.
nous blood; (4) a venous system with an unpaired ventral Therefore, if we wish to identify the nearest living rela-
vein; (5) well-developed blood vessels in the dermis; (6) tives of Recent amphibians, lungfishes probably are a
telolecithal development of jelly-coated bipolar eggs; (7) justifiable choice. On the assumption that Recent am-
ciliated larvae; and (8) presence of a glottis, epiglottis, phibians are descended from labyrinthodonts, it follows
flask glands, pituitary structure and a tetrapod neurohy- that the nearest relatives of these fossil taxa are dipnoans
pophysial hormone, lens proteins, bile salts, and certain also. On the other hand, if we restrict ourselves only to
gilí arch muscles. fossil taxa for the analysis of relationships in the manner
Most fishes and most tetrapods have a genome size of of Schultze (1981) and others, we are asking a different
3-10 picograms of DNA per diploid nucleus (Morescal- question: What is the nearest relative of the most primi-
chi, 1977). The major exceptions to this generalization tive known tetrapod, currently considered to be Ichthy-
are salamanders and dipnoans. Most salamanders have ostega? The paleontologist must rely on the fossil record
30-86 pg per nucleus, bul members of the oblígate neo- with its acknowledged limitatíons, and the evidence to
tenic families have 91-192 pg per nucleus, an amount date (Schultze, 1981) suggests that osteolepiform fishes
exceeded only by lungfishes (160-284 pg per nucleus). are more closely allied to labyrinthodont amphibians thars
However, there seems to be no phylogenetíc significance are dipnoans.
 Origin and Early Evoluüon
Both phylogeneüc schemes are hypotheses and, as such, short compared with the facial región (Figs. 15-2, 15-6, 435
they cannot be proven to be true, only shown to be and 15-17). A columella or stapes lay laterally adjacent
incorrect. There are two ways in which to falsify any to the auditory capsule in the región of the cheek or otíc
hypothetical scheme of genealógica! relationships. The notch, and the skull articulated with the vertebral column
first involves demonstrating that one or more of the as- by means of a double occipital condyle. Some of these
sumptions on which the scheme is based is incorrect. In changes can be related to a shift to terrestrial locomotion,
this case, both phylogenies are based on the same sct of air breathing, and the obvious premium that would have
assumptions (see D. Rosen et al., 1981, for list). The been placed on the development of sensory systems
second way to invalídate a phylogenetic arrangement is adapted to terrestrial rather than aquatic habitáis. Al-
to prove that the postulated sequence of character trans- though we cannot be sure, the shape of the skull suggests
formation has been misinterpreted—i.e., that characters that primitive amphibians uülized a force-pump respira-
considered to be homologous are not. This, in fact, ac- tory mechanism involving contractions of the mandibular
counts for the current controversy. A few examples will musculature to draw air through the nostrils into the buc-
suffice. D. Rosen et al. (1981) considered the excurrent cal cavity and thence into the lungs. A broad, fíat, rigid
narial opening of lungfishes to be homologous with the skull would seem to be architecturally advantageous for
internal choana of tetrapods; Schultze (1981) did not. this mechanism. Because the nostrils and associated ol-
The authors disagree about the homologies of the dermal factory organs served the dual purpose of air intake and
bones of the tetrapod skull table, the tetrapod limb bones, olfaction, one would expect an elaboration of the snout
and those of the maxillary arch in dipnoans, as well as región that might have been accomplished by a posterior
the significance of tooth histology. Selection of one phy- shift in the orbits. Such a shift might have occasioned
logenetic scheme in preference to the other becomes an expansión of preorbital bones (e.g., prefrontal) and
exercise in deciding which author(s) interpreted the evo- repression of postorbital bones (e.g., postorbital and
lutionary sequence of character transformation more ac- postfrontal). Given the flattening of the head, the eyes
curately. As new data are secured and oíd evidence rein- carne to be located dorsally. Once on land, the amphib-
terpreted, these phylogenetic arrangements possibly will ians required a more sensitive sound-amplifying device.
be modified and perhaps even rejected in favor of alter- Henee, the stapes (derived from the hyomandibular bone
native schemes. Thus, the question of the origin of am- of fishes) acted as a transmitter from the external surface
phibians remains a challenge to biologists. of the head (presumably modified as a tympanic mem-
brane or eardrum) in the región of the otic notch to the
auditory capsule via the oval window (fenestra ovalis).
DIVERSITY AND EVOLUTION The development of double occipital condyles would have
OF EARLY TETRAPODS allowed movement of the head in a dorsoventral plañe;
Settíng aside now the problematic issue of the origin of this, in combination with autostylic jaw suspensión, would
primitive tetrapods, we can address the amazing radiaüon have facilitated a snap-and-grab mechanism of feeding.
of these ancient amphibians throughout the latter part of Modificaüons of the axial and appendicular skeleton
the Paleozoic (Carboniferous and Permian) and the are associated with terrestrial rather than aquatic loco-
Triassic. During these 120 million years, the primitive motor habits. The flexible notochord was supplemented,
amphibians must have exploited the terrestrial environ- and ultimately replaced, by blocks of cartilage and bone
ments within the bounds of their physiological limitaüons along its length. The vertebrae formed by these cartílagi-
(moisture being a criücal factor then, as it is for modern nous and bony blocks took on a diversity of morpho-
amphibians). Their first significan! terrestrial competitors logical types, ranging from "arch" to "husk" structures
probably were reptiles, which are thought to have ap- (Fig. 15-4). Regardless of the form, the funcüon was sim-
peared near the middle of the Carboniferous. In the ilar—i.e., to provide an axial element strong enough to
meanüme, amphibians must have competed with a vast withstand resistance to the contraction of appendicular
array of freshwater and marine fishes. Seemingly all and trunk muscles in the terrestrial médium, which ob-
primitive amphibians were predaceous; some must have viously provided much less support than the aquatic mé-
preyed on fishes (both freshwater and marine), others on dium. Robust, bicapitate ribs were attached to the trunk
small amphibians, and some of the smaller types on aquatic vertebrae to form a thoracic basket, within which internal
and terrestrial invertebrates. organs were protected (Fig. 15-5). Moreover, the well-
developed, oblique ribs suggest that costal ventilaüon was
Adaptations to Terrestriality a primitive feature of early amphibians. The pectoral gir-
The morphological features that disünguish tetrapods from dle, freed of its bony attachment to the rear of the skull,
their predecessors (see the earlier section: The Nature of provided a frame suspended by musculature with which
a Tetrapod) can be interpreted as adaptations to in- the anterior limbs articulated. The pelvic girdle was sus-
creased terrestriality. The skull tended to become freely pended from the axial column via an artículation between
movable on the trunk, broad, fíat, and rigid; the snout the now prominent dorsal iliac processes and specially
became elongate and the otíco-occipital región relatívely modified sacral ribs. The primitive finlike appendages were
EVOLUTION
436

Figure 15-17. Diversity in cranial architecture

among labyrinthodont amphibians.
A. Loxomma, dorsal view. B. Trematosuchus.
dorsal view. C. Eogyrínus, ventral view.
D. Trematosuchus, ventral view. Orbits, nares,
and palatal vacuities are hatched. Note positions
and shapes of orbits in A and B, and
interpterygoid vacuities in D. A and C redrawn
from Panchen (1980); B and D redrawn from
Romer (1947).

modified to include elbow and knee joints as torques would facilítate swallowing. Skin glands and a well-de-
were applied to the limbs in terrestrial locomotion. Re- veloped lymphaüc system would have been ¡mportant in
sistance for forward thrust on land was provided by the keeping the skin moist for cutaneous respiration and for
pentadactyl hand and foot. diminishing desiccaüon. The eye must have undergone
Although the fossil record provides no evidence of the some striking modifications, developing a convex cornea,
soft anatomy of these primitive amphibians, we can as- flattened lens, and a mechanism to move the lens to
sume that the transiüon to terrestrial habits must have accommodate visión in air. Similarly, removed from the
occasioned some striking modifications. For example, in aquatic médium, the eye must be protected; thus it is
order to feed out of water, the development of a tongue reasonable to assume that these organisms might have
would have helped to secure prey and manipúlate and had eyelids, lubricaüng glands, and the ability to with-
swallow it. Also, mucous-secreüng intermaxillary glands draw the eye at least parüally into the head.
 Origin and Early Evolution
Groups of Primitive Amphibians pond-dwelling animáis represented by Dip/ocau/us with 437
Classically, these tetrapods are divided into two sub- broad, fíat bodies and "horned" skulls.
classes, the Labyrinthodontia and the Lepospondyli, on A third group, the microsaurs (e.g., Euryodus), were
the basis of the arch vertebrae of the former and husk included formerly with the aistopods and nectrideans, but
vertebrae of the latter. The labyrinthodonts are common the microsaurs differ from these groups in having a small
as Late Paleozoic and Triassic fossils and are representad intercentrum. Furthermore, they are more generalized and
by two orders, the Anthracosauria and the Temnospon- characterized by an elongate trunk, weak limbs, three-
dyli. The primary distinction between these two groups digit manus, and a skull in which the supratemporal is
lies in the structure of their arch vertebrae. In anthraco- retained but the intertemporal and tabular are lost. This
saurs the pleurocentrum tends to become the dominant group is importan! because it has been postulated by
element in the centrum, whereas in temnospondyls it is some authors to be ancestral to both salamanders and
the intercentrum that dominates. Additionally, anthra- caecilians.
cosaurs are characterized by a moderately large tabular
bone that articulates with the parietal, whereas in tem-
nospondyls the bone is small and has no contact with STATUS OF THE LISSAMPHIBIA
the parietal. The anthracosaurs, which became extinct at Since Gadow (1901) first proposed the infraclass Lissam-
the cióse of the Permian, were represented by two phibia to include the three Recent amphibian orders—
groups—the water-dwelling embolomeres (e.g., Palaeo- salamanders, caecilians, and anurans—the relationships
herpeton; Fig. 15-2), and the more terrestrial seymour- of these groups to one another and to various fossil taxa
iamorphs that have a large otic noten and a single occip- have been the subject of continual, and at times, heated
ital condyle. debate. A minority of scientists (e.g., Herré, 1935; Carroll
In contrast to the anthracosaurs, the temnospondyls and Currie, 1975; and Carroll and Holmes, 1980) have
persisted into the Triassic. It is in this latter group that we hypothesized sepárate origins for all three orders. An-
note a tendency for the skull to become flattened and other group has suggested that although salamanders and
reduced through the loss of bone (intertemporal lost; caecilians share a common ancestor, anurans were de-
tendency for braincase to be cartilaginous; pterygoid re- rived independently; included here are Romer (1945),
duced resulting in interpterygoid vacuities; tabular small), Holmgren (1952), von Huene (1956), J. Lehman (1956),
and to develop double occipital condyles (Fig. 15-17). and Jarvik (1942, 1960, 1980-81). Schmalhausen (1958,
The temnospondyls are represented by a variety of adap- 1959) and Nieuwkoop and Sutasurya (1976) postulated
tive types ranging from specialized, long-snouted marine independent origins of anurans and salamanders but did
fish-eaters (e.g., Trematosaurus) to heavier-bodied, more not comment on the position of the caecilians. Among
generalized forms such as Edops. The more primitive those who believed salamanders and anurans share a
temnospondyls are represented by the suborder Rha- common ancestor, with caecilians having been derived
chitomi (e.g., Eryops), in which a pleurocentrum still per- separately, are Haeckel (1866), Noble (1931b), Eaton
sists along with the intercentrum. Among the rhachitomes (1959), and Reig (1964). Pusey (1943) and N. Stephen-
was a group of small terrestrial animáis, the dissorophids, son (1951a, 1951b, 1955) supported the monophyly of
from which some or all of the modern amphibians may salamanders and anurans, but did not comment on the
have arisen. More advanced temnospondyls are repre- status of caecilians. Finally, some authors—H. Parker
sented by the stereospondyls (e.g., Rhinesuchus), in which (1956), Szarski (1962), Parsons and E. Williams (1963),
pleurocentra and skulls are much reduced, and the pal- Estes (1965), Jurgens (1971), Morescalchi (1973), Bolt
atal dentition is arranged in long rows of teeth smaller (1977, 1979), Gardiner (1983)—supported the mono-
than the large tusks characteristic of more primitive phyleüc origin of the three orders. To attempt a critical
temnospondyls. The third group of temnospondyls are review of all of this literature would be cumbersome here.
the highly specialized plagiosaurs (e.g., Plagiosaurus), Instead, the reader is directed to the excellent summaries
which are thought to be neotenic. These animáis have of pre-1962 papers in Szarski (1962) and Parsons and
broad, short skulls and peculiar, elongate vertebrae. E. Williams (1963). The more recent contributions are
The second major group of primitive tetrapods is rep- reviewed here and integrated with the aforementioned
resented by two orders—the Aistopoda and Nectridea. syntheses.
Unlike the labyrinthodonts, these animáis with husk-type
vertebrae diversified into a variety of small forms, pri- Origin of the Lissamphibia
marily in the Carboniferous; none is known later than Among those authors who favor a monophyletic origin
the Permian. The aistopods (e.g., Ophiderpeton) are of the three orders or a common ancestor for anurans
strange snakelike creatures with limbs reduced or lost and and salamanders, there is general agreement that this
up to 200 vertebrae. Nectrideans are represented by two ancestor is to be found among the temnospondylous am-
types—a limbless, or nearly limbless, eel-like animal with phibians. Gardiner (1983) Usted four synapomorphies of
a long, pointed skull (e.g., (Jrocordy/us), and the bizarre, temnospondyls and Recent amphibians: (1) skull lacking
EVOLUTION
438 premaxilla-
nasal —

maxilla-
lacrimal
prefrontal
palatine
sphenethmoid
frontal Ij
pterygoíd—j*L
jugal
postfrontal
: •^ 'I postorbital
-"•-parietal
squamosal

Figure 15-18. Skuil of the -quadratojugal—-L'

temnospondylous dissorophid
amphibian Doleserpeton annectens in
A. dorsal and B. ventral views.
-quadrate T
Redrawn from Bolt (1977). — postparietal parasphenoid

an intemasal bone; (2) possession of labyrinthodont teeth; Bolt (1977) argued for a paedomorphic origin of the
(3) presence of small apical fossa with vomers that meet lissamphibians from the dissorophids on the grounds that
premaxillae anteriorly; and (4) infraorbital canal looped it is a recognized evolutíonary mode among Recent sal-
over lacrimal bone and continuous over jugal and lacri- amanders and among some labyrinthodonts (Boy, 1972,
mal bones. Even among authors who favor a polyphy- 1974). Because of the small size of Recent amphibians,
letíc origin of the Lissamphibia, there is a general con- Bolt (1979) reasoned that progenesis is the most logical
sensus that anurans are allied closely with temnospondyls mechanism for their origin. Following S. Gould (1977),
of the family Dissorophidae that range from the Middle Bolt suggested further that a progenetíc origin of lissam-
Pennsylvanian to the Lower Triassic. These amphibians phibians from the terrestrially adapted dissorophids en-
were small, terrestrial organisms with a primitive amphib- abled them to reproduce rapidly in ephemeral aquatíc
ian biphasic life cycle (Bolt, 1979). The appendicular environments and, as small-sized adults, exploit a variety
skeleton was well developed and the body relaüvely short of suitably moist terrestrial microhabitats—a strategy
(26 or fewer presacral vertebrae). Cranially, dissorophids characteristic of many groups of Recent amphibians. Bolt's
lack an intertemporal bone and have a large orbit and arguments are strengthened further by his observations
an otic notch (Figs. 15-18, 15-19). The maxillary arch is that the juvenile dissorophid, Doleserpeton, possesses
complete, with the maxilla articulaüng with the quadra- pedicellate palatal teeth, and that the earliest known dis-
tojugal. The occipital condyles are paired, and a hypo- sorophid, Amphibamus grandiceps (Fig. 15-19), as an
glossal foramen in the exoccipital presumably provided adult possesses Do/eserpeton-like juvenile dentítion.
an exit for the eleventh and twelfth cranial nerves pos- Moreover, their palatal tooth arrangement resembles that
terior to the skull. of lissamphibians. Bolt (1979) also reasoned that the os-
Bolt (1977, 1979) suggested that lissamphibians may sified vertebral centra of Doleserpeton (consisting of a
have arisen from dissorophids via progenesis, a hetero- cylindrical pleurocentrum that may or may not be com-
chronic shift in the rate of ontogenetic development that plete dorsally and a small crescentric intercentrum) may
results in paedomorphosis—an evolutíonary mechanism be ontogenetíc precursors of the ossified rhachitomous
in which larval and/or juvenile characters of the ancestor centra of Amphibamus and other dissorophids (Fig. 15-
are retained in subadult and adult stages of the descend- 19).
ant. Progenesis involves precocious sexual maturity ac- Nearly all proponents of polyphyletic origins of the
companied by an arrest of the rate of growth and change Lissamphibia have sought the origins of salamanders and
of body shape. The process should not be confused with caecilians from one or more of the lepospondylous am-
a second heterochronic pattern, neoteny, that also results phibians, owing principally to the superficial similarity be-
in paedomorphosis. Neoteny involves retardation of so- tween the husk-type vertebrae of these primitive am-
maüc development with respect to sexual maturation, or phibians and those of the modern salamanders and
retardation of both sexual and somatic development. caecilians. Only the nectrideans and microsaurs have been
 Origin and Early Evolutíon
premaxilla- 439
septomaxilla

^r nasal
^-lacrimal vomer
prefrontal
palatine
frontal
sclerotic ring
postfrontal
maxilla

parietal
pterygoid

quadratojugal

^"occiput" epipterygoid—'
-quadrate parasphenoid—'
-jugal stapes—'
postorbital

"occiput"
nasal Figure 15-19. Skull of the
temnospondylous dissorophid
quadrate premaxilla amphibian Amphibamus grandiceps
in A. dorsal, B. ventral, and
quadratojugal 1 —lacrimal C. lateral views. Redrawn from Bolt
jugal—' '—maxilla (1979).

considered seriously as possible ancestors to salamanders Carroll and Holmes (1980) proposed that on the basis
and/or caecilians. Gregory et al. (1956) postulated that of the structure of the cheek and temporal región, mi-
salamanders were derived from nectrideans; these is some crosaurs and salamanders share a similar pattern of ad-
evidence to support this (Gardiner, 1983), but there is ductor jaw muscles; thus, they suggested that the ances-
some convincing counterevidence (Parsons and E. Wil- tors of anurans and salamanders diverged from one
liams, 1963). The primary characters that are contrain- another in the early Carboniferous, with salamanders
dicaüve of a cióse relationship are the absence of: (1) evolving from microsaurs and anurans from labyrintho-
pedicellate teeth, (2) operculum and otic notch, and (3) donts in the Late Permian and Triassic. The evidence for
short, broad skull. As a group, nectrideans tend to have microsaurs or nectrideans as ancestors to any groups of
elongate bodies. The neural and haemal arches of the modern amphibians is weak by comparison with the evi-
vertebrae possess unique striatíons unknown in modern dence supporting a dissorophid ancestor, because the
amphibians, and the vertebrae tend to have unique ar- latter evidence consists almost entirely of primitive resem-
ticulating processes. blances.
The microsaurs have been postulated to be ancestral
to salamanders and caecilians most recently by Carroll Modern Amphibians
and Currie (1975) and Carroll and Holmes (1980). Mi- Parsons and E. Williams (1963) and Gardiner (1982,
crosaurs resemble modern salamanders in possessing bi- 1983) concisely interpreted the evidence for the mono-
capitate ribs and in not having lost any of the dermal phyly of the three orders of living amphibians. Using Par-
cranial elements typical of primitive Recent taxa. On the sons and Williams's outline, we elabórate on the char-
other hand, an oüc notch is absent, as is an articulation acters, incorporatíng and adding new or contradictory
between the maxilla and quadratojugal. On the basis of information that bears on the subject.
similarities of the skull roof, palate, and braincase in cae-
cilians and the Paleozoic microsaur Gonior/iynchus, Car- Characters Uniquely Linking the Three Recent
roll and Currie (1975) suggested that caecilians were de- Amphibian Orders. Several character complexes are
rived independently of salamanders and anurans, and common to all three living orders:
possibly are allied to a Goníor/iynchus-like microsaur. 1. Pedicellate teeth.—In the majority of Recent am-
EVOLUTION
440 fossil salamanders (Estes, 1975). The significance of this
crown variation is not entirely clear. In the frog Ceratophrys,
J. Lehman (1968) demonstrated that the undivided teeth
outer margin of jaw develop secondarily from divided teeth. However, Lar-
sen (1963) noted that the larval salamanders that he ex-
pedicel amined had undivided teeth, and that divided teeth did
not appear until the larvae transformed. Thus, the pres-
ence of undivided teeth in salamanders probably is a
paedomorphic trait in contrast to their presence in anu-
rans which seems to be a derived specialization.
Although the presence of this unique tooth structure
has long been known in Recent amphibians (first noted
by Leydig, 1867), it was not known to occur in any fossil
groups until reported for the Lower Permian temno-
anterior- spondyl Doloserpeton annectens (Dissorophidae) by Bolt
(1969). Subsequently, Bolt (1979) demonstrated that the
palatal teeth of most adult dissorophids are conical and
sharp-pointed—i.e., typical labyrinthodont fanglike teeth.
However, juvenile Doloserpeton have pedicellate (and
probably bicuspid) palatal teeth, and the Middle Penn-
sylvanian dissorophid Amphibamus gmndiceps has ped-
icellate, bicuspid marginal teeth (palatal teeth unknown).
2. Operculum-plectrum complex.—Despite the
statement of Carroll and Currie (1975) with regard to
replacement crown
caecilians, it seems fairly certain that the majority of am-
growing up from phibians possess a columella (plectrum) and operculum
within pedicel to transmit sounds to the inner ear, although the two
elements are fused in some taxa (see Chapter 13). The
distal element, the columella, is derived phylogenetically
from the hyoid arch and is invariably present in sala-
manders and caecilians. It is attached distally in cartilage,
Figure 15-20. Pedicellate teeth in Lissamphibia. A. Salamander bone, or connective tissue with the squamosal or quad-
(Amphiuma means). B. Caecilian (Dermophis mexicanas).
C. Anuran (Caudiverbera caudiverbera). Drawn from photographs rate, or the hyoid. In some anurans, the columella is lost
in Parsons and E. Williams (1962). (Trueb, 1973, 1979), but in the majority that possess it,
the columella is united to the external tympanum (absent
in caecilians, salamanders, and some anurans) by the
phibians having teeth, the teeth consist of a basal pedicel cartilaginous pars externa plectri derived from the pala-
and a distal crown (Fig. 15-20). Both are composed pri- toquadrate (Barry, 1956). The operculum develops in
marily of dentine, with the dentine of the pedicel and association with the fenestra ovalis in all amphibians, ex-
crown being divided by uncalcified dentine (some anu- cept oblígate neotenic salamanders in which it presum-
rans) or a ring of fibrous connecüve tissue (salamanders, ably has been lost (see Chapter 6). In salamanders, the
caecilians, other anurans). Generally the crown is shorter operculum and columella are sepárate or fused; in most
than the pedicel and is capped by enamel or an enamel- anurans, they are syndesmotically united, and in caeci-
like material. The boundary between the crown and the lians they are thought to be fused synostotically into a
pedicel, which is composed of cement, lies cióse to the single unit.
gum line. Developmentally, both parts of the tooth arise 3. Papilla amphibiorum.—All amphibians possess a
as a continuóos layer of tissue separated in the early specialized and unique sensory área in the wall of the
stages from the bones of the jaw; the inner surfaces of sacculus in the inner ear (see Chapter 14 for a descrip-
both the crown and pedicel are lined with prominent tion). The function of the papilla amphibiorum is to re-
odontoblasts (Parsons and E. Williams, 1963). Among ceive acoustic signáis of less than 1,000 Hz, whereas a
the few amphibians that are known to lack pedicellate second sensory área, the papilla basilaris, receives sound
teeth are salamanders of the genus Siren, and frogs of frequencies of more than 1,000 Hz.
the genera Phyllobates and Ceratophrys. The separation 4. Green rods.—Both salamanders and anurans have
between the crown and the pedicel tends to be obscured a special type of visual cell in the retina, the "green rods,"
in some specimens of salamanders of the genera Nec- that are unique to these two groups (Walls, 1942). The
turus and Proteus, in the anuran genus Bombina (Par- function of these cells is unknown, and apparently they
sons and E. Williams, 1963), and in some paedomorphic are absent in caecilians, which characteristically have greatly
 Origin and Early Evolutíon
reduced eyes that, for all practical purposes, are non- cavity. This force-pump mechanism characterizes all Re- 441
funcüonal as sight organs in adults. cent amphibians and clearly is quite inefficient given the
5. Structure of m. levator bulbi.—Of the eight eye considerable amount of energy expended to secure a
muscles, seven are innervated by branches of Cranial relatively small amount of oxygen, in contrast to the sys-
Nerves III, IV, and VI, whereas only one, the m. levator tems of amniotes and air-breathing fishes. The intemal
bulbi, is innervated by a branch of Cranial Nerve V. This surfaces of the lungs of Recent amphibians are poorly
muscle consists of a thin sheet that forms an elastic floor developed, lacking the spongy surface characteristic of
to the orbit, lying between the eye and the roof of the amniotes.
mouth. Its primary functíon seems to involve elevating 9. Chromosomes and DNA contení.—Karyologi-
the eye (an ability unique to amphibians), thereby en- cally the modern groups of amphibians are characterized
larging the buccal cavity to facilítate respiraüon. The mus- by (1) the tendency to acquire through evoluüon karyo-
cle is structurally similar in anurans and salamanders. Al- types composed of reduced numbers of chromosomes,
though the posterior part is reduced in caecilians, the all metacentric and differing little in size; (2) the tendency
anterior part is homologous to that in anurans and sal- to increase the amount of DNA (genome size), especially
amanders (Reig, 1964). The modification of this muscle in salamanders, but also in anurans and caecilians; and
in caecilians is not surprising in view of the reduction of (3) notable interspecific variability in genome size even
the eye and complete dermal roofing of the skull. among related species having morphologically similar
6. Fat bodies.—All three orders are characterized by karyotypes (Morescalchi, 1973, 1980) (see Chapter 16
fat bodies associated with the gonads. Although their shape for details). These patterns are in marked contrast to all
varíes, the fat bodies similarly develop from the germinal other groups of vertebrales.
ridge and therefore seem to be homologous in anurans, 10-14. Other Characters.—Among the synapomor-
salamanders, and caecilians. phies listed by Gardiner (1983), the following are in-
7. Structure of skin glands.—All Recent amphibians cluded here: (10) roofing bones in temporal región con-
have two kinds of skin glands—mucous and granular (or sisting of parietals only; (11) craniovertebral joints similar;
poison) glands. The similarity of their structure in the (12) short ribs not encircling body; (13) musculocuta-
three orders substantíates their homology. neous vein present; and (14) postfrontal bone absent.
8. Respiratory mechanisms and attendant special-
izations.—A peculiarity of all Recent amphibians is their Characters of Recent Amphibians that Occur in
reliance on cutaneous respiratíon facilitated by the main- Other Tetrapods. Some characters that are shared by
tenance of a moist skin surface by the numerous mucous the three Recent groups of amphibians also occur in some
glands for the transfer of oxygen. Presence of dermal skin other groups of tetrapods.
coverings and reduced numbers of mucous glands pre- 1. Fenestration of the temporal región of the skull.—
clude this mode of respiratíon in amniotes, which instead In primitíve amphibians the orbit is bounded ventrally
have perfected a respiratory mechanism that relies pri- and posteroventrally by the jugal and postorbital bones,
marily on the action of intercostal muscles (among other respectively, that sepárate the orbit from the temporal
specializations) to modérate the air pressure in the lungs región. Both the jugal and the postorbital are absent in
and a sophisticated vascular system to distribute oxygen- all Recent amphibians. Salamanders and most anurans
ated blood to the tissues. This contrasts with the circu- are alike in possessing a fenestrate temporal región in
latory system in amphibians in which a three-chambered which the side of the skull ventral and posteroventral to
heart incompletely sepárales venous and arterial blood, the orbit is open but bounded ventrally to some degree
and the organisms' reliance on a force-pump mechanism by the maxillary arch. A number of anurans have elabo-
to Ínflate the lungs. rated dermal bone in the temporal región, thereby re-
Whereas aquatic vertebrales that breathe with lungs ducing the fenestraüon secondarily (Trueb, 1973). Among
use the pressure of the surrounding water to forcé air into these is a wide array of casque-headed species of hylid
the lungs, amphibians inspire air into the buccal cavity and bufonid frogs that have elaborated the dermal roof-
by lowering the floor of the mouth while the nostrils re- ing bones for purposes of protectíon and/or external sup-
main open. As the floor is raised, air is expelled. After port. In carnivorous anurans (of which there are repre-
several such oscillatory cycles, the nares are closed and sentatíves in the hylids, leptodactylids, and ranids), the
the larynx opened, at which time some air from the lungs elaboration of bone in the temporal región nearly covers
mixes with that ¡n the buccal cavity. As the floor of the the adductor jaw musculature. All of these are camivores;
mouth is elevated when the nostrils are closed, some of therefore, as in the case of the casque-headed species,
the contents of the buccal cavity are forced by differentíal the elaboration of bone in the temporal región seems to
pressure into the lungs and trapped there by the closure be a derived feature associated with specialized habits.
of the larynx. Subsequent opening of the nostrils and Likewise, the caecilians as a group lack temporal fenes-
movement of the floor of the mouth expels air from the tratíon. This can be viewed as one of a suite of cranial
buccal cavity. As the larynx opens and the body wall modificatíons associated with the burrowing habits of the
muscles contract, air flows from the lungs into the buccal order. In the case of the caecilians, this specialization
EVOLUTION
442 cervical vertebra, or atlas, characteristically bears double
tympanum cotyles and lacks transverse processes or ribs.
5. Morphology of nasal región.—On the basis of de-
tailed studies of the snout regions of anurans, salaman-
ders, Poro/epis, and Eusthenopteron, Jarvik (1942) pos-
stapes
tulated a basic dichotomy whereby porolepiforms were
ancestral to salamanders that have widely separated na-
middle-ear sal capsules and osteolepiforms (Eusthenopferon) gave
cavity rise to anurans characterized by medially adjacent nasal
quadrate capsules. On the basis of an exhaustivo study, Jurgens
(1971) showed that the medial separatíon of the nasal
1 capsules is variable in salamanders and anurans, de-
¡ss Eustachian
tube pending on ontogenetic development. During develop-
articular ment the forebrain is retracted from the internasal región;
the more nearly complete the retraction, the closer the
nasal sacs (and capsules) approximate one another me-
dially. Retraction is most marked in caecilians and in ad-
vanced anurans, and least marked in primitive anurans
(e.g., Ascaphus and Leiopelma) and salamanders, which
Figure 15-21. Cross section of half of an amphibian skull in the resemble one another closely.
ear región showing the dorsal orientation of the stapes from the Jurgens (1971) also demonstrated that the three orders
fenestra ovalis of the inner ear to the tympanum distally. Redrawn share other features in common. The ontogeny of the
from Romer (1945).
nasal sacs is the same, with the observed differences being
expressions of the stage at which ontogénesis is termi-
nated. The openings in the nasal capsule (i.e., foramen
(along with the others) is a feature common to all mem- apicale of salamanders and caecilians, and fenestra na-
bers of the group. Altematively, Carroll and Currie (1975) sobasalis of anurans) for the branches of the ramus
suggested that the lack of temporal fenestration (along ophthalmicus profundus nerve are homologous. Jacob-
with some other cranial characters} allies caecilians more son's organ is homologous in salamanders and anurans,
closely with the microsaur Goniorhynchus than with either and possibly in caecilians also, although in that group the
salamanders or frogs. However, Goniorhynchus retains association of the organ with the tentacular apparatus
jugal, postorbital, and temporal bones, whereas caecili- represents a specialization that obscures its primary con-
ans do not; the ventral and posteroventral margins of the dition. All three orders possess homologous intermaxil-
orbit are formed by the maxilla and squamosal, and the lary glands.
expanded squamosal covers most of the temporal región 6. Position of stapes.—Among temnospondyls for
laterally. which there are data and all Recent amphibians, the stapes
2. Loss of posterior skull bones.—All Recent am- (= columella) is dorsolaterally directed from the fenestra
phibians lack the supratemporal, intertemporal, tabular, ovalis (Fig. 15-21). The element is directed ventrolater-
and postparietal bones of the posterior skull table char- ally in higher vertebrales and in osteolepiform fishes.
acteristíc of primitive amphibians.
3. Advanced type of palate.—In primitive tetrapods Equivoca! features of modern amphibians. Some
the pterygoids are in cióse contact or approximate each features of modern amphibians are insufficiently known
other anteromedially. Posteromedially, they articúlate (but to determine if they characterize the group as a whole or
do not fuse) with the braincase via a basipterygoid artic- not.
ulaüon. The medial part of the parasphenoid, the cultri- 1. Vertebral column.—Owing to the lack of fossil evi-
form process, is a slender element, lies free dorsal to the dence, the homologies of vertebral centra in Recent am-
pterygoids, and does not articúlate with the vomers. In phibians (and tetrapods as a whole) are unknown (see
contrast, Recent amphibians are characterized by ptery- [> Wake, 1970, for review of the literature and discus-
goids that are separated widely and reduced, and that sion). The vertebrae of the three orders of living am-
almost always articúlate with the braincase. The cultri- phibians are exclusively monospondylous; the neural arch
form process of the parasphenoid tends to be moderately usually is fused to the centrum, initial vertebral ossifica-
broad to wide, never underlies the pterygoids, and oc- tion appears in the intermyotomal recess, and some de-
casionally arüculates with the vomers (especially in sal- gree of ossification from the perichordal tube occurs in
amanders and caecilians). each order. Vertebral development in the three groups
4. Presence of double occipital condyles.—In all follows three quite disünct patterns (D. Wake, 1970). Thus
modern amphibians the skull articúlales with the verte- in salamanders, the centrum is derived from hypertro-
bral column by means of two occipital condyles. The first phied intervertebral cartilage (formed in the perichondral
 Origin and Early Evolution
tube surrounding the notochord) and the cartílage found future nervous system, the entire chordal and prechordal 443
within the notochord in midvertebral and intervertebral mesoderm, and most of the endoderm (Nieuwkoop and
áreas. In contrast, the majority of the centrum in caeci- Sutasurya, 1976). A third pattern of mesoderm formation
lians is derived from membranous additions. Interverte- was reported by R. E. Keller (1976) for the frog Xenopus
bral cartílage is reduced; it forms a ligament joining ad- laevis. In this species the mesoderm is double-layered,
jacent centra and contributes bone to the ends of the lies in the deep layer of the marginal zone (i.e., covered
centra. Notochordal tíssue is limited to the intervertebral by the suprablastoporal endoderm—the prospective en-
cartílage that underlies the cartilaginous rudimento of the dodermal archenteron roof); as mesoderm is involuted
neural pedicel. Anurans are characterized by two patterns over the lip of the blastopore, it moves along the inner
of vertebral development, perichordal and epichordal. In surface of the deep layer of ectoderm toward the animal
the former mode, the cartílage vertebral model ossifies pole. At ¡ts upper extent the mesoderm, with the deep
membranously around the notochord, reducing the size layer of the prospective neural and epidermal ectoderm,
of the notochord and frequently obliteratíng it. Epichor- consists of the prospective notochord dorsally, flanked
dal formation is characterized by ossification of the tíssue by prospective somite and lateral mesoderm. Further re-
dorsal to the notochord; the notochord itself, as well as search on amphibians probably will yield further variation
the cells lateral and ventral to it, degenerate and disap- in the topography and morphogenetic movements of the
pear. With the exception of the primitive frogs, noto- primary anlagen, but to date too little is known to justify
chordal tíssue does not persist in anurans. phylogenetic speculations on the significance of these dif-
2. Mesoderm formation and formation of primor- ferences.
dial germ cells.—In the few species for which there are
data (e.g., the salamander Triturus and the frogs Bom- Monophyly of the Lissamphibia. Clearly, the
bina and Xenopus), significan! variation has been found monophyletic origin of the Recent amphibians cannot be
in the mode of mesoderm formation. Nieuwkoop and defended unequivocally, although the accumulated evi-
Sutasurya (1976) reported that in the blastula-early gas- dence seems to support this hypothesis. The issue is
trula stage the prospective mesoderm and adjacent su- obfuscated by the quality of the existing data. The fossil
prablastoporal endoderm occupy the superficial cell layer record is mediocre for salamanders and anurans and vir-
in the marginal zone, which ¡s externa! in Triturus. In tually nonexistent for caecilians. Many of the characters
contrast, the marginal zone in Bombina is exclusively in- that unite the three orders are features of the soft anat-
fernal. Because the blástula of Triturus is single-layered, omy that are not preserved in the fossils. And finally,
the presence of surface mesoderm is associated with the there remains a great deal to be learned about the mor-
occurrence of a rupture discontinuity in the superficial phology and development of modern amphibians in gen-
layer between the presumptíve endoderm and meso- eral, and caecilians in particular. Progress, if it is to be
derm, as the mesoderm is brought into its definitive po- made, lies in the pursuit of specific and detailed studies
sition between endoderm internally and ectoderm exter- in these áreas. And syntheses that address the phyloge-
nally during gastrulatíon (R. E. Keller, 1976). In the double- netic relatíonships of amphibians are only relevant to the
layered blástula of Bombina, the superficial cells give rise degree that they (1) consider the greatest number of
to the ectodermal epithelial layer of the epidermis, the characters possible, (2) establish the evoluflonary polar-
ependymal layer of the central nervous system, and ities of the characters, (3) intégrate features of fossil and
the endodermal inner lining of the archenteron (¡.e., the Recent amphibians, and (4) justify the exclusión of con-
primitive gut); the inner layer of cells gives rise to the tradictory evidence.
presumptíve sensorial layer of the epidermis, most of the
 CHAPTER 16
The Amphibia seem to be confronted by
two contrasting genetic demands, namely
to maintain a high degree of heterozygosity
implying an adaptive fimction and to keep
unaltered some relative linkage-groups,
also ofan adaptive valué acquired over
Cytogenetic,
long evolutionary periods.
Atessandro Morescalchi (1979) Molecular;
and Genomic
Eiolution

T he ways in which genotypes are maintained within

populations and species and the mechanisms by which
Chromosome Number and Structure
The karyological characterisücs distinguishing amphibi-
changes occur in speciation and in the evolution of lin- ans from other classes of vertebrales are (1) a tendency
eages are fundamental problems in evolutionary biology. toward genome hypertrophy, (2) a high degree of DNA
Since about 1960, there have been great advances in spiralizaüon, and (3) great interspecific differences in the
the fields of cytogeneücs and molecular genetics. A pro- amounts of nuclear DNA. The earlier ideas about relative
liferation of new techniques and their continued refine- conservativeness of chromosome morphology in the de-
ment have permitted geneticists to make new kinds of rived families in each order (e.g., Morescalchi, 1973) have
observations, which have led to a much better under- been contradicted by more data on diverse taxa.
standing of the processes of genic evolution. Gross morphological differences in chromosomes in-
clude size and centromeric position. Relative sizes gen-
erally are designated as microchromosomes and macro-
CYTOGENETICS chromosomes. Microchromosomes are extremely small
Amphibians are exceptionally good organisms for kary- and possibly may be confused with so-called supernu-
ological studies because most have few, comparatively merary or accessory chromosomes, which may be vari-
large chromosomes. Most of the work on amphibian cy- able in their presence or number (Morescalchi, 1973; D.
togenetics has been with conventionally stained chro- Green et al., 1980). Macrochromosomes commonly can
mosomes; this kind of material allows the determination be grouped into large or small chromosomes, but in some
of size, centromeric position, secondary constrictions, and taxa there is a gradual change in size. Chromosomes are
percentage lengths of chromosomes and their arms (see classified in relation to the position of the centromere
Morescalchi, 1973, for a review). Newly developed tech- along the length of the chromosome (Levan et al., 1964).
niques, as used by O. Ward (1977), M. Schmid (1978a, Chromosomes having the centromere in the median re-
b), M. Schmid et al. (1979), Veloso and Iturra (1979), gión are termed metacentric. A submetacentric position
and Vitelli et al. (1982), have provided an insight into denotes that the arms are unequal in length, and the
the chromosomal location of constitutive heterochro- shortest arm is above the centromere. A chromosome
matin, nucleolus organizer regions, and ribosomal RNA having the centromere in a terminal position is termed
genes (see Birstein, 1982, for summary). telocentric and one with the centromere near the end,

445
EVOLUTION
446 subtelocentric. Centromeric position determines the are known (Table 16-2). The diploid number of chro-
number of arms on the chromosome (telocentrics have mosomes ranges from 66 ¡n the hynobiids Onychodac-
only one, whereas others have two). The number of arms tylus japonicus and Ranodon sibiricus to 22 in New World
sometimes is called the nombre fundamental (NF). salamandrids. With the exception of sirenids, which may
Quantitative analytical procedures are being developed be polyploid, the highest number of chromosomes and
for karyotypic comparisons (D. Green et al., 1980). the greatest number of microchromosomes occur in the
In the following sections the karyotypes of the three Cryptobranchoidea. Ambystomatids and plethodontids
living orders of amphibians are summarized. This survey have only 13 or 14 pairs of chromosomes and completely
is followed by discussions of sex chromosomes and poly- lack microchromosomes. Salamandrids have 11 or 12
ploidy. pairs that gradually grade from macro- to microchro-
mosomes, as they do in amphiumids, which have 14
Caecilians. Karyological data are available for few pairs. Proteids are intermedíate between cryptobran-
species of caecilians (Table 16-1), and the absence of choids and other salamanders in having 19 pairs of chro-
data on chromosomal banding precludes detailed com- mosomes, of which 1 pair is classified as microchromo-
parisons. There is a general trend from a high number somes in Necturus.
of chromosomes (2N = 42) and many microchromo-
somes (30) in primiüve caecilians to fewer chromosomes Anurans. Several hundred species in diverse genera
(2N = 20-24) and no microchromosomes in advanced representing all families of anurans have been karyotypes
caecilians (Nussbaum, 1979a). However, some presum- (Table 16-3). Supposed microchromosomes have been
ably derived karyotypes are associated with primiüve found only in members of primitive families: Ascaphus
morphological and life history traits among caeciliids (e.g., truei, Leiopelma hochstetíeri, and Discoglossus pictus.
Caecilia and Siphonops). Addiüonally, some morpholog- However, the small chromosomes in Leiopelma may be
ically derived caeciliids have 4 or 5 pairs of microchro- supernumerary chromosomes (Morescalchi, 1980), and
mosomes (M. Wake et al., 1980), but none approaches trióse in Ascaphus may not be microchromosomes
the higher numbers (7—15 pairs) of microchromosomes (D. Green et al., 1980). With the exception of Xenopus,
of the ichthyophiids. Clearly, the paucity of data pre- the basic karyotype of other anurans seems to be 26 bi-
cludes any well-supported hypothesis on karyological ev- armed chromosomes. Xenopus tropicalis has only 20
olution within caecilians, even though a general trend chromosomes; the several species of Xenopus having 36
does seem to be apparent. chromosomes may be the result of an ancient polyploid-
ization (W. Müller, 1977).
Salamanders. The extensive literature on the karyol- Diverse lineages of anurans show a reduction from the
ogy of salamanders was summarized by Morescalchi basic number of 26 chromosomes. This is especially evi-
(1975). The chromosomes of about 90% of the genera dent in the Leptodactylidae, Hylidae, and Ranidae, and

Table 16-1. Chromosomes of Caecilians

Diploid Pairs of macro-'
Species number microchromosomes Reference
Ichthyophiidae
Ichthyophis beddomei" 42 6/15 Seshacher (1937)
Ichthyophis glutinosas 42 10/11 Nussbaum and Treisman (1981)
Ichthyophis kohtaoensis 42 10/11 Nussbaum and Treisman (1981)
Ichthyophis orthoplicatus 42 10/11 Seto and Nussbaum (1976)
Uraeotyphlus menoni 36 11/7 Elayidom et al. (1963)
Uraeotyphlus narayani 36 8/10 Seshacher (1939)
Caecilüdae
Caecilia occidentalis 24" 12/0 Barrio and Rinaldi de Chieri (1970a)
Dermophis mexicanas 26 8/5 M. Wake and Case (1975)
Gegeneophis camosus 30 5/10 Seshacher (1944)
Geotrypetes seraphini 38C 15/4 Morescalchi (1973); Stingo (1974)
Grandisonia altemans 26 12/1 Blommers-Schlosser (1978)
Gymnopis multiplicata 24,26 8/4,5 M. Wake and Case (1975)
Hypogeophis rostratas 26 12/1 Nussbaum (1979a)
Siphonops paulensis 24 12/0 Barrio and Rinaldi de Chieri (1972)
Typhlonectidae
Chthonerpeton indistinctum 20 10/0 Barrio et al. (1971)
Typhlonectes compressicauda 28 14/0 M. Wake et al. (1980)
"Reported as Ichthyophis glutinosus; see Seto and Nussbaum (1976).
^Also reported as 22 (M. Wake and Case, 1975).
cAlso reported as 36 (M. Wake and Case, 1975).
 Cytogenetic, Molecular, and Genomic Evolution
Table 16-2. Chromosomes of Salamanders" 447
Diploid Pairs of macro-/ Nuclear DNA
Taxonomic group number microchromosomes (pg/N)6
Hynobiidae
Onychodacíy/us japonicus >66 21/>11 ±100
Ranodon sibiricus 66 14/19 51
Batrachuperus mustersi 62 12/19 43
Salamandrella fceyser/ingi 62 19/12 42
Hynobius Hchenatus 60 19/11 —
Hynobius (11 species) 56 18-20/8-10 33-41
Hynobius retardatus 40 20/0 38
Cryptobranchidae
Andrias and Cryptobranchus 60 15/14-15 93-112
Sirenidae
Pseudobranchus striatus (4N ?) 48/64 24^2/0 91
Siren lacertina (4JV ?) 52 26/0 114
Siren intermedia (4N ?) 46 23/0 108
Salamandridae
Oíd World (11 genera, 20 species) 24 12C 39-67
Notophthalmus viridescens 22 ll c 63-86
Taricha (3 species) 22 ll c 56-60
Proteidae
Proteus anguinus 38 19/0 97
Necturus (5 species) 38 18/1 160
Amphiumidae
Amphiuma (2 species) 28 14C 130-192
Dicamptodontidae
Rhyacotriton 26 13/0 120
Dicamptodon 28 14/0 -
Ambystomatidae
Ambystomad 28 14/0 48-103
Plethodontidae
Desmognathines (2 genera, 3 species) 28 14/0 30-40
Hemidactylines (3 genera, 5 species) 28 14/0 35-71
Plethodontines (3 genera, 8 species) 28 14/0 39-86
Hydromaníes (5 species) 28 14/0 -
Bolitoglossines (7 genera, 17 species) 26 13/0 84e
"Based primarily on Morescalchi (1975) and Morescalchi et al. (1977, 1979).
^Diploid cells; picograms (1U
"uiploíd (10~12
"• g) per nucleus.
nucleus.
cMacrochromosomes gradually decreasing to microchromosomes.
^Exclusive of triploids.
eOne species.

is characteristic of all bufonids. The reduction presumably centric fission or dissociation of metacentric chromo-
has occurred, not through the loss of genomic material, somes is implicated in the formation of telocentric chro-
but by the rearrangement of the material by centric fu- mosomes. Fission or dissociation may be modified further
sión, especially of the smaller telocentric chromosomes by pericentric inversión and translocation (Bogart, 1973,
(Morescalchi, 1973). Thus, there seems to be a general 1981). Species in derived families having more than 26
trend in some anuran lineages for reduction in the num- chromosomes commonly have a corresponding number
ber of chromosomes and formation of bi-armed chro- of telocentric chromosomes. The diploid number of chro-
mosomes. Reduction is extreme in some African ranids; mosomes in most hylines, including Osteopilus septen-
there are eight pairs of chromosomes in some species of trionalis, is 24. One species, Osteopilus brunneus, has
Phrynobatrachus and Cardioglossa and only seven pairs 34, 20 of which are telocentric and compare with the 20
in Arthroleptis (Bogart and Tandy, 1981). arms of metacentric chromosomes in O. septentrionales
In some groups of frogs the basic number of 26 chro- (C. Colé, 1974). The extreme diploid number of 54 is in
mosomes is increased. For example, the primitive genera the African ranid Astylostemus diadematus; most of its
of hylids have 26 chromosomes, and although most Hyla chromosomes are telocentric (Bogart and Tandy, 1981).
and related genera have 24 chromosomes, many neo-
tropical Hyla (the H. leucophyllata complex) have 30. Chromosomes and Sex Determination
The genus Eleutherodactylus has a great range (18-36) There is no uniform type of geneüc sex determination in
of chromosomes. Many of the 30-chromosome Hyla and amphibians. Sex reversal experiments showed female
Eleutherodactylus with high numbers of chromosomes heterogamy in Xenopus laevis (M. Chang and Witschi,
have one or more pairs of telocentric chromosomes. Thus, 1956), mPleurodelespoiretiandP. waltl (Gallien, 1954),
EVOLUTION
44o Table 16-3. Chromosomes of Anurans
Diploid
Taxonomic group number Reference
Leiopelmaüdae
Ascaphus truei 46" D. Creen et al. (1980)
Leiope/ma hochstetteri 22-30" E. Stephenson et al. (1972, 1974)
Leiopelma archeyi and hamiltoni 18 E. Stephenson et al. (1972, 1974)
Discoglossidae
Alytes obstetricans 38" Morescalchi (1973)
Discog/ossus picrtfs 28 Morescalchi (1973)
Bambino (3 species) 24 Morescalchi (1973)
Rhinophrynidae
Rhinophrynus dorsalis 22 C. Colé (1971)
Pipidae
Xenopus (6 species)' 36 Tymowska (1977)
Xenopus tropicalis 20 Tymowska (1973)
Hymenochirus boettgeri 24 Morescalchi (1981)
Pipa carvalhoi 20 Morescalchi (1981)
Pipa pipa 22 Morescalchi (1981)
Pipa pama 30 Olmo and Morescalchi (1978)
Pelobatidae
All genera and species, 26 Morescalchi et al. (1977)
except Leptolalax pelodytoides 24 Morescalchi et al. (1977)
Pelodytidae
Pe/odytes punctatus 24 Morescalchi et al. (1977)
Myobatrachidae
All genera and species, 24 Morescalchi and Ingram (1974, 1978)
except 4 species of Limnodynastes 22 Morescalchi and Ingram (1974, 1978)
Sooglossidae
Nesomantis and Soog/ossus 26 Nussbaum (1979b)
Heleophrynidae
Heleophryne 26 Morescalchi (1981)
Leptodactylidae
Ceratophryinaeb 26 Barrio and Rinaldi de Chieri (1970c); Begak et al. (1970)
Telmatobiinae
Eupsophus 28, 30 Bogart (1970); Barrio and Rinaldi de Chieri (1971)
Other genera 26 J. D. Lynch (1978)c
Odontophryninib 22 Saez and Brum-Zorrilla (1966)
Grypiscini 26 Becak et al. (1970); Bogart (1970)
Eleutherodactylini
Eleutherodactylus 18-36 Morescalchi (1979); Bogart (1981)
Sminthillus limbatus 32 Bogart (1981)
Synhophus (2 species) 26, 30 Bogart (1973)
Holoaden bradei 18 deLucca et al. (1974)
Other genera 22 J. D. Lynch (1971Y
Hylodinae
Crossodacty/us and Hy/odes 26 Begak (1968); Denaro (1972)
Leptodactylinae
Limnomedusa (1 species) 26 Barrio (1971)
Adenomera (2 species) 26 Bogart (1974)
Adenomera marmorata 24 Bogart (1974)
Paratelmatobius íuízi 24 deLucca et al. (1974)
Pseudopaludicola (2 species) 18-22 Brum-Zorrilla and Saez (1968)
Lithodytes Hneatus 18 Bogart (1974)
Other genera6 22 Morescalchi (1979)c
Bufonidae
All genera and species,6 22 Bogart (1972)
except Bufo regularía groupb 20 Bogart (1972)
Brachycephalidae
Brachycephalus ephippium 22 Bogart (pers. comm.)
Rhinodermatidae
Rhinoderma (2 species) 26 Formas (1976b)
"Part of the complement consiste of pairs of microchromosomes: Ascaphus, 5/18 pairs of macro-/microchromosomes; Leiopelma hochstetteri,
11/0-8; Alyies, 11/8 (D. Creen et al., 1980, offered a different explanation).
In addition to the diploid numbers given, some species are poiyploids.
cReferences to various genera and species included in these summaries.
dSeveral species of Kaloula, includmg pulchra, reported as having 28 chromosomes, but K. pulchra also reported to have only 24 by Bogart and
C. Nelson (1976).
 Cytogenetic, Molecular, and Genomic Evolution
449
Diploid
Taxonomic group number Refercnce

Pseudidae
Pseudis paradoxa 24 Barrio and Pistol de Rubel (1970)
Hylidae
Pelodryadines, 26 Menzies and Tippett (1976); Morescalchi (1979)
except Litaría tnfrafrenata 24 Menzies and Tippett (1976)
Phyllomedusines'' 26 P. León (1970); Bogart (1973)
Hemiphractínes
Fritziana (3 species) 26-30 Bogart (1973)
Gastrotheca (12 species) 26, 28 Bogart and Duellman (unpublished)
Other genera and species 26 Bogart (1973); Duellman and Hoogmoed (1984)
Hylinae
Osteopi/us brunneus 34 C. Colé (1974)
Hy/a "¡eucophytlata complex" 30 Bogart (1973); Duellman and Trueb (1983)
Acn's crepitans 22 C. Colé (1966)
Other genera and speciesb 24 Morescalchi (1979)c
Centrolenidae
Centrolenella 20 Bogart (1973)
Dendrobatidae
Colostethus 24 Bogart (1973)
Dendrobates (6 species) 18-22 P. León (1970); Bogart (pers. comm.)
Ranidae
Raninaeb 26 Morescalchi (1979); Bogart and Tandy (1981)
except Píychadena (5 species), 24 Bogart and Tandy (1981)
Rana (3 species), 24 Kobayashi (1963)
and ñaña kuhlii and namiyei 22 Kuramoto (1972, 1980)
Petropedetinae
Anhydrophryne and Petropedetes 26 Bogart and Tandy (1981)
Dimorphognathus africanus 24 Bogart and Tandy (1981)
Phrynobatrachus (6 species) 16-20 Bogart and Tandy (1981)
Mantellinae
All genera and species, 26 Blommers-Schlosser (1978)
except some Mantidacíy/us 24
Arthroleptínae
Arthro/eptis (3 species) 14 Bogart and Tandy (1981)
Cardiog/ossa (2 species) 16 Bogart and Tandy (1981)
Astylosterninae
Astylostemus diadematus 54 Bogart and Tandy (1981)
Nycfibates cormgaíus 28 Bogart and Tandy (1981)
Hemisinae
Hemisus (1 species) 24 Bogart and Tandy (1981)
Hyperolüdae
All genera and species, 24 Blommers-Schlosser (1978);
except Lepíopefe (10 species) 22, 24, 30 Bogart and Tandy (1981)
Rhacophoridae
All genera and species 26 Kuramoto (1977); Morescalchi (1981)
Microhylidae
Asterophryinae 26 C. Colé and Zweifel (1971)
Genyophryninae 26 C. Colé and Zweifel (1971)
Phrynomerinae 26 Morescalchi (1981)
Dyscophinae 26 Blommers-Schlosser (1976)
Cophylinae 26 Blommers-Schlosser (1976)
Microhylinae
Kaloulad 28 Kuramoto (1980)
Other Asian genera 26 Natarajan (1953)
G/ossostoma and Otophryne 26 Bogart and C. Nelson (1976); Bogart et al. (1976)
Chiasmoc/eis 24 Bogart and C. Nelson (1976)
Other New World genera 22 Bogart and C. Nelson (1976)
EVOLUTION
450 Male heterogamy (XY/XX type) has been found in three
anurans—Rana escalenta (Schempp and M. Schmid,
1981), Eupsophus migue/i (Iturra and Veloso, 1981), and
Gastrotheca riobambae (M. Schmid et al., 1983); several
salamanders—five species of Necturus (Sessions and J.
Wiley, 1985), Triturus alpestris, T. helveticus, and T. vul-
garis (M. Schmid et al., 1979); and various species of
bolitoglossine plethodonüds (Dendrotriton, Nototriton,
Oedipina, and Thorius) (P. León and Kezer, 1978).
Female heterogamy (ZZ/WZ type) has been noted for
certain in one anuran, Pyxicephalus adspersus (M. Schmid,
1980), and possibly in Discoglossus pictus (Morescalchi,
1964), and in several salamanders: Pleurodeles poireti
(Lacroix, 1970), P. waltl (Lacroix, 1968), Triturus cris-
tatus (Callan and L. Lloyd, 1960), T. marmoratus (Man-
cino and Nardi, 1971), Siren intermedia (P. León and
Kezer, 1974), Ambystoma laterale (Sessions, 1982), and
Aneides ferreus (Kezer and Sessions, 1979).
No sex chromosomes have been identified in caecili-
ans. Presumably the type of chromosomal heterogamy
will be determined for many species of amphibians in the
future through modern staining techniques and by gene
linkage-group studies using gel electrophoresis. Possibly
w X 4 Y X chromosomal heterogamy is not the mechanism for de-
termining the sexes in all amphibians, for no sex chro-
Figure 16-1. Heteromorphic sex chromosomes ¡n amphibians.
A. Pyxicephalus adspersus, ZZ/ZW type (M. Schmid, 1980). mosomes have been identified in several amphibians,
B. Rana escalenta, XX/XY type (Schempp and M. Schmid, 1981). including Xenopus laevis, which has been studied thor-
C. Necturus maculosus, XX/XY type (Sessions, 1980). Different oughly (Tymowska, 1977). Although different morphol-
shading represents differentially stained bands; numbers refer to
chromosome pair. All redrawn to approximately same scale. ogies and banding patterns (and therefore differential
replicating DNA) have been identified, the causal factors
for XY/XX and ZZ/WZ heterogamy have yet to be de-
in Ambystoma mexicanum and A. figrinum (Humphrey, termined. However, it is now known that ribosomal RNA
1945), and in Bufo bufo (Ponse, 1942). On the other not only is a component of the nucleolus organizer re-
hand, similar experiments and investigations of partheno- gions but also occurs at other sites; the inheritance of
genetically bred frogs indicated male heterogamy in these chromosomal sites follows simple Mendelian prin-
Bombina orientalis, Hyla japónica, and four species of cipies (Batistoni et al., 1978). Furthermore, in snakes
Rana (brevipoda, japónica, nigromaculata, rugosa) (Ka- having ZZ/WZ heterogamy (Singh et al., 1976), it has
wamura and Nishioka, 1977), and also in R. pipiens (C. been shown that there is differential satellite DNA asso-
Richards and Nace, 1978). Studies on the expression of ciated with the W and Z chromosomes. Possibly the ori-
the gene for the H-Y cell surface antigen have confirmed gin of satellite DNA in the W chromosome is the first step
female heterogamy in Xenopus laevis and indicated male in the differentiation of the sex chromosomes by gener-
heterogamy in Rana pipiens (Wachtel et al., 1975). Sex- aüng asynchrony in the DNA replication pattern of Z and
linked genes for enzymes have been detected in Pleu- W chromosomes. Conceivably this reduces the fre-
rodeles waltl (Ferrier et al., 1980) and in hybrids of Rana quency of crossing-over, which is the prerequisite of dif-
catesbeiana andR. clamitans (Elinson, 1981). Sex-linked ferentiation of sex chromosomes.
genetic loci have been identified in R. pipiens. In Rana,
sex is determined by a locus or a small región of the Polyploidy
chromosome; the rest of the "X" and "Y" chromosomes The addition of one or more haploid chromosome com-
apparently are identícal (D. Wright et al., 1983). plements to the normal diploid genome occurs naturally
Relatívely new techniques for the staining of constitu- in several species of salamanders and anurans (Table 16-
tive heterochromatin, ribosomal proteins, and replicating 4). These polyploid species or populations generally are
chromosomal DNA have provided a way to identify sex associated with their supposed ancestral diploid popula-
chromosomes other than by gross morphology, as was tions. With the possible exception of the sirenids, there
done with Discoglossus pictus (Morescalchi, 1964). The are no known polyploid families, genera, or even species
cytological evidence for the few species in which sex groups of amphibians (see Bogart, 1980, and Kawamura,
chromosomes have been identified shows heteromorphic 1984, for reviews). Polyploidy can be induced in eggs
chromosomes by gross morphology and/or banding pat- prior to the second meiotic división by temperature shock
terns; these fall into two types (Fig. 16-1). or elevated pressures in the laboratory (Ferrier and Jay-
 Cytogenetic, Molecular, and Genomic Evolution
Table 16-4. Occurrence of Polyploidy in Amphibians 451
Zygote
Species production Ploidy Reference
Salamanders
Ambystoma p/at/neum Gynogenetíc 14 x 3 = 42 Uzzell (1963)
Ambystoma tremblayi Gynogenetic 14 x 3 = 42 Uzzell (1963)
Ambystoma íexanum x laterale Gynogenetic/ 14 x 3 = 42 Downs (1978)
?parthenogenetíc
Pseudobranchus striatus Bisexual polyploid 16 x 4 = 64 Morescalchi and Olmo (1974)
Siren lacertina Bisexual polyploid 13 x 4 = 52 Morescalchi and Olmo (1974)

Anurans
Xenopus ruwenzoriensis Bisexual polyploid 18 x 6 = 108 Fischberg and Kobel (1978)
Xenopus uestitus Bisexual polyploid 18 x 4 = 72 Tymowska and Fischberg (1973)
Xenopus sp. Bisexual polyploid 18 x 4 = 72 Fischberg and Kobel (1978)
Neobatrachus sudelli Bisexual polyploid 12 x 4 = 48 Mahoney and Robertson (1980)
Neobatrachus sutor Bisexual polyploid 12 x 4 = 48 Mahoney and Robertson (1980)
Ceraíophrys aurita Bisexual polyploid 13 x 8 = 104 Becak et al. (1967)
Ceratophrys ornato Bisexual polyploid 13 x 8 = 104 Be9ak et al. (1966)
Odontophrynus americanus* Bisexual polyploid 11 x 4 = 44 Bogart (1967)
Pleurodema bibronü Bisexual polyploid 11 x 4 = 44 Barrio and Rinaldi de Chieri (1970b)
Pleurodema kriegi Bisexual polyploid 11 x 4 = 44 Barrio and Rinaldi de Chieri (1970b)
Bufo danatensis Bisexual polyploid 11 x 4 = 44 Pisanetz (1978)
Bufo uiridis* Bisexual polyploid 11 x 4 = 44 Mazik et al. (1976)
Bufo sp. Bisexual polyploid 10 x 4 = 40 Bogart and Tandy (1976)
Hy/a versicolor Bisexual polyploid 12 x 4 = 48 Wasserman (1970)
Phylhmedusa burmeisteri* Bisexual polyploid 13 x 4 = 52 Batistic et al. (1975)
Dicroglossus occipitalis Bisexual polyploid 13 x 4 = 52 Bogart and Tandy (1976)
Rana escalenta* Hybridogenetic 13 x 3 = 39 R. Günther (1975a)
Tomopíema delalandü* Bisexual polyploid 13 x 4 = 52 Bogart and Tandy (1976)

*Some populations are diploid and others polyploid.

let, 1978); also foreign or irradiated spermatozoa may are broadly sympatric with R. esculenta, a hybrid "spe-
actívate development of gynogenetíc diploid eggs that cies," diploids of which contain one set of chromosomes
have been subjected to temperatura or pressure shock from each of the parental species. Ova of R. esculenta
(Nace et al., 1970; Volpe, 1970). Polyploidy in amphib- fall into distinct size classes; the large eggs develop into
ians was reviewed by Bogart (1980). triploids. If these eggs are fertilized by R. lessonae, the
Polyploidy in amphibians may be the result of hybrid- genotypes of the offspring are composed of two sets of
ization of two or more species (allopolyploidy) or may R. lessonae chromosomes and one set of R. ridibunda
have occurred spontaneously in a single species (auto- chromosomes. On the other hand, if the eggs are fertil-
polyploidy). Multívalent associations (more than two ho- ized by R. esculenta or R. ridibunda, the genotypes of
mologous chromosomes in synapsis) during meiosis have the offspring contain one set of R. lessonae chromosomes
bcen used as evidence for chromosomal homology; thus, and two sets of R. ridibunda chromosomes. Presumably,
a polyploid having multivalents is assumed to be an au- diploid eggs are produced by diploid R. esculenta, but
topolyploid. Because hybrid sets of chromosomes are not individual females may produce both haploid and diploid
homologous, allopolyploids form few, if any, multiva- eggs (Uzzell et al., 1975). Crossing triploids results in
lents. However, multivalents can be expected only in a phenotypes of all three taxa (Berger, 1977).
recent autopolyploid, for polyploid species probably go On the basis of the progeny from numerous matings
through stages of diploidization as the number of muta- (but without cytological documentatíon), the process of
tions accumulates; eventually the polyploid has fewer and premeiotic endomitosis has been inferred to occur in Rana
fewer multivalents. Presumably most, if not all, polyploid esculenta for the production of diploid ova (Uzzell et al.,
species of amphibians are allopolyploids. In many cases 1977). In this system in diploid H. esculenta, the genomes
the polyploids exist in at least partial sympatry with closely are segregated so that the R. ridibunda or R. lessonae
related diploid congeners (e.g., tetraploid Hyla versicolor genome ends up in the first polar body. The first polar
with diploid H. chrysosce/is; octoploid Ceratophrys or- body is eliminated, and the remaining R. ridibunda or R.
nata with diploid C. cranwelli). lessonae genome passes through a second meiotíc equa-
The hybridogenetic populations of Rana esculenta in tional división and remains intact in the ovarían nucleus.
Europe provide a fascinating natural experiment in poly- Some multivalents and bridges occur in meiosis in male
ploidy. The extensive literature on this complex of species R. esculenta, thereby suggesting genetic recombination
has been reviewed by Berger (1977), Dubois (1878), and between nonsister homologues (R. Günther, 1975b).
Hotz and Bruno (1980). Rana ridibunda and R. lessonae Salamanders of the Ambystoma jeffersonianum com-
EVOLUTION
452 A. jeffersonianum - female A. jeffersonianum
^—
Jz A. platineum

Figure 16-2. Hypothetical

hybridization event in the origin of Jw Lz
O
the triploid species in the
Ambystoma jeffersonianum complex.
J = A. jeffersonianum chromosome D ploid female
complement; L = A. laterale hybrid
chromosome complement; w =
femaie sex chromosome; z = male
sex chromosome. Arrow desígnales
chromosomal reduplication in
oogénesis. Adapted from Sessions
(1962). A. laterale - male

plex occur in the Great Lakes región in North America; tineum; these offspring have karyotypes idéntica! to those
the complex consists of two bisexual diploid species (A. of A. jeffersonianum.
jeffersonianum and A. laterale) and two all-female triploid Mixed populations of all-female diploid and triploid
species (A. platineum and A. tremblayi) (Uzzell, 1964). Ambystoma occur on the Bass Islands in Lake Ene. These
Detailed cytological studies on these salamanders (Ses- presumably are hybrids between A. laterale and A. tex-
sions, 1982) revealed that the triploid species are allotri- anum, with triploids having two sets of chromosomes of
ploids with complementan; karyotypes and identifiable A. texanum (Downs, 1978). Because no males are known
sex chromosome heteromorphism of the WZ-female/ZZ- to occur on North Bass Island, the all-female Ambystoma
male type. The hybrid origin of the triploid species hy- on that island may be parthenogenetic.
pothesized by Sessions (1982) is one involving a female Although experimental evidence is lacking, at least two
A. jeffersonianum and a male A. laterale that resulted in species of sirenid salamanders may be tetraploids (More-
a diploid female hybrid, in which a prediplotene meiotic scalchi and Olmo, 1974; Morescalchi, 1975). This hy-
reduplication occurred during oogénesis. This resulted in pothesis is based on chromosome structure and the ab-
the productíon of diploid ova. Such ova fertílized by sperm sence of microchromosomes, but there is no published
of A. jeffersonianum resulted in the allotriploid A. plati- evidence for the formation of quadrivalents during meiosis.
neum having two complements of A. jeffersonianum
chromosomes and one of A. laterale; fertilization by A. Meiotic Chromosomal Structure
laterale resulted in the allotriploid A. tremblayi having Cytological studies of meiotic processes have revealed
one complement of A. jeffersonianum chromosomes and some apparent differences in the morphological charac-
two of A. laterale (Fig. 16-2). teristics of the bivalents in different groups of amphibians.
This model is parsimonious because it necessitates re- The lampbrush chromosomes (diplotene) are reasonably
duplication only once in the history of the complex. Fur- well known in salamanders, especially through the pi-
thermore, it explains the all-female populations of the oneering efforts of Kezer and Macgregor (1971), who
triploid species, because sex determination in Ambys- identified centromeric heterochromatin and provided a
toma is the dominant-W {female heterogamy) type foundation for investigations of DNA replication with re-
(Humphrey, 1945). The triploid species uülize the actí- spect to chromosome structure. Interspecific differences
vation properties of sperm of diploid males to initiate occur in the spiralization of the bivalents and in the po-
zygote development; A. platineum uses sperm of A. jef- sition of the chiasmata, and in some salamandrids, dif-
fersonianum, and A. tremblayi uses sperm of A. laterale. ferences exist in the frequency and position of chiasmata
The mechanism of sperm rejection is unknown, but be- between the sexes (Morescalchi, 1973).
cause the triploid ova is in homologous balance chro- Within the salamanders the bivalents generally have
mosomally, a penetratíng sperm nucleus, although re- more than two chiasmata, interstitial in position. Two pat-
quired for activation of the egg, would be rejected as part terns are evident in the anurans (Morescalchi, 1973):
of the physiological reaction to supernumerary sperm In the Leiopelmatidae and Discoglossidae the diplo-
characteristic of most salamanders (Sessions, 1982). tene stage of Late Prophase I is long with a short diaki-
Breakdown of the sperm rejection mechanism results in nesis; the bivalents have relatively little spiralization. There
tetraploids, as in female A. tremblayi inseminated by A. are more than two chiasmata in the large bivalents but
laterale males discovered by Sessions (1982), who also only one in the small bivalents. Most chiasmata are in-
noted that apparent failure of oocyte chromosomes to terstitial, and at Metaphase I chiasmata terminalization is
reduplícate results in diploid offspring by triploid A. pla- never total.
 Cytogenetic, Molecular, and Genomic Evolution
ln the other families of anurans, the diplotene stage of thus, anurans that have rapid embryonic development in 453
Late Prophase I is short with a relatively long diakinesis; temporary ponds tend to have the lowest amounts of
the bivalents are highly spiralized. Usually there are two nuclear DNA, and those that have prolonged develop-
chiasmata in both large and small bivalents, and usually ment in cold water have large genomes. The genome
the chiasmata are terminal. Exceptions include Pipa parva size in species in the humid tropics is near or above the
and some neotropical hylids having bivalents with inter- mode for anurans.
stitíal (procentric) chiasmata, and some African ranoids Within anurans and salamanders, there is a positive
having bivalents with proterminal chiasmata in late diplo- correlation between genome size and nuclear volume,
tene and diakinesis. cell volume, and cell surface área of erythrocytes (Olmo
Variable numbers of chiasmata and chromosome mor- and Morescalchi, 1975, 1978), but there are differences
phology have been reported in two species of caecilians between anurans and salamanders and between oblígate
i Sungo, 1974; Seto and Nussbaum, 1976); available data neotenic salamanders and other salamanders. This is
are inadequate to make generalizations about caecilians. especially evident between genome size and relative cell
However, the morphology of meiotic chromosomes of surface área (Fig. 16-3). The valúes for anurans are lower
salamanders and primitive families of anurans is similar, than, but parallel to, those of non-neotenic salamanders,
and different from that of the more advanced families of but there is great variatíon in large amounts of DNA in
anurans. the large cells (with low surface-area/volume ratíos) in
the oblígate neotenic salamanders. In anurans and non-
neotenic salamanders, the correlaüon between genome
MOLECULAR EVOLUTION size and relative cell surface área seems to be under the
Recent technological advances have provided biologists same mechanistic control. Thus, the genome size and cell
with the opportunity to utilize macromolecules in evolu- volume/surface ratios seem to be indicative of physiolog-
tíonary studies. These approaches include gel electro- ical adaptations to various environmental conditions.
phoresis of proteins, microcomplement fixation of serum However, qualitaüvely, the differences in cellular and nu-
albumins and hemoglobin, immunodiffusion, and se- clear sizes among amphibians seem to be associated with
quencing of nucleoenzymes, proteins, DNA, and RNA. the more repetitive (nongenic) DNA fractions (Mizuno et
Amphibians have figured prominently in these molecular al., 1976).
studies, which have provided new insights into evolu- The fací that most salamanders have far more DNA
tíonary mechanisms, as well as phylogenetic relation- than anurans may relate to different adaptive strategies
ships. in the two orders and certainly relates to the duraüon of
embryonic development (see Chapter 5). According to
Cenóme Size and Characteristics Ohno (1970), the large quantities of DNA in salaman-
The amount and replication sequences of nuclear DNA ders, especially the oblígate neotenes, may have been
are highly variable among amphibians. Little is known acquired through tándem duplicaüon of the structural genes
about caecilians; three taxa have 7.4—27.9 picograms of alone, which, by synthesizing great quantities of the same
nuclear DNA per diploid nucleus (Morescalchi, 1973). proteins, would lead to larger cell sizes. These large cells
Anurans have 2-36 pg/N (Morescalchi, 1977), whereas would require ever greater quantities of the same gene
salamanders have much greater amounts, 33-192 pg/N producís and therefore the continuous activity of the du-
(Table 16-2). The salamanders fall into two distinct plicated genes. As a result, these salamanders cannot
groups—normally metamorphosing, primarily terrestrial elimínate genetic redundancy. Ohno (1970) suggested
taxa having 33-86 pg/N, and oblígate neotenic salaman- that for this reason salamanders are "evolutionarily ster-
ders having 91-192 pg/N. ile."
The modal genome size in anurans is 9 or 10 pg/N (K. Perhaps the oblígate neotenic salamanders are evo-
Bachmann and Blommers-Schlósser, 1975). K. Bach- lutionary dead ends, but certainly this cannot be said for
mann et al. (1972) suggested that each group of organ- some other groups, especially the bolitoglossine pletho-
isms has a minimal amount of DNA representing the ge- dontids, which have relatively large amounts of DNA.
netic information necessary for expressing the group- Furthermore, the generalized quantification of genomes
specific characteristícs; the amount of DNA beyond this does not take into account the different components of
minimum codes for the species-specific characters. Fur- DNA that have greatly different degrees of repetitiveness.
thermore, high valúes of DNA provide a reservoir of raw As an example, DNA hybridization studies of 15 species
material for production of new genes. Generalized spe- otPIethodon (Mizuno and Macgregor, 1974) showed (1)
cies of anurans usually have genome sizes near the mode, salamanders in the same species group had 60-90% of
whereas highly specialized species tend to have ex- observed repetitive DNA sequences in common; (2) two
tremely low or high amounts of DNA (K. Bachmann and species groups in eastern North America shared 40-6Q%
Blommers-Schlósser, 1975). Another interpretation cen- of the sequences; and (3) eastern and western North
ters around the positive correlaüon between genome size American species had less than 10% of the sequences in
and rate of embryonic development (K. Bachmann, 1972); common.
EVOLUTION
454

150-

_
O
5

§100
O)
o
o

50-

Figure 16-3. Relationship between

the ratio of cell surface área to cell
volume and nuclear DNA contení.
Triangles are anurans; open circles
are non-neotenic salamanders, and
soiid circles are oblígate neotenic Q5 1.0 1.5 2.0 2.5
salamanders. Adapted from Olmo
and Morescalchi (1978). Cell surface/Cell volume

Comparison of DNA reassociatíon and genome size in (Schmidtke et al., 1976). The tetraploid Hyla versicolor
two anurans (Xenopus laevis and Bu/o bu/o) and two has about twice the amount of DNA as its presumed
salamanders (Necturus maculosus and Triíurus cn'status) diploid ancestor but has an equal amount of RNA (K.
by Baldan and Amaldi (1976) revealed that each of the Bachmann and Bogart, 1975).
species had about the same absolute amount of unique Although the amount of information accumulated on
DNA. The differences in total nuclear DNA in these spe- genome size and on DNA replication since the mid-1979s
cies were accounted for by quanütative variations of the is impressive, patterns are only beginning to emerge. It
repetitive sequence classes, at least in part because of seems that the DNA content is significant, not only in a
changes in the numbers of copies of the various se- genetic informational context, but also with respect to
quences. Moreover, these authors suggested that the great cellular metabolism and rate of embryonic development,
differences ¡n amounts of nuclear DNA between sala- both of which may be modified evolutionarily in response
manders and anurans involve all sequence classes in par- to the environment. Thus, genome size might increase
allel. as a protective adaptaüon to the higher mutation rate
The variation in the amount of nuclear DNA in closely necessary for evolution, the higher information redun-
related species is especially obvious in salamanders (Table dancy buffering the effect of somatic mutations. There-
16-2). Moreover, among salamanders there seems to be fore, both genome size and mutation rate would change
no correlation between the diploid number of chromo- under selective pressures.
somes and the genome size. For example, three species
of Tañería have 22 chromosomes and 56-60 pg/N of Ribosomal RNA
DNA, whereas five species of desmognathines have 28 The nucleolar organizer región (ÑOR) is the región of the
chromosomes but only 30-40 pg/N of DNA. On the other chromosome that produces the nucleolus. In ¡nterphase
hand, interspecific differences in genome size are closely through late prophase, these regions lack DNA but are
correlated with the number of chromosomes in Xenopus rich in RNA. The nucleolar organizer is a differentíated
(Thiébaud and Fischberg, 1977). Xenopus tropicalis región of chromatin (DNA), which, through transcription,
(2N = 20) has only 3.55 pg/N of DNA, whereas species produces the larger pieces of RNA—i.e., 18S and 28S
having 2N = 36 chromosomes have 6.35-8.45 pg/N. ribosomal RNA (rRNA)—that are incorporated into the
Two tetraploid species (4N = 72) have 12.57-12.83 pg/ ribosomes. However, other regions of the genome pro-
N, and one octoploid species (8N = 108) has 16.25 pg/ duce the 5S rRNA and code for the ribosomal proteins.
N. Likewise, tetraploid populations of the frog Oc/onío- Quantítative relationships exist between the amounts
phrynus americanus have a nuclear DNA content of 7.1 of chromosomal DNA and rDNA (the DNA sequences
pg/N, whereas diploid populations have 3.6 pg/N coding for 18S + 28S rRNA together with intervening
 Cytogenetic, Molecular, and Genomic Evolution
spacer sequences). DNA-rRNA hybridization in three produce about 280 times more rDNA than is known in 455
species of anurans and nine of salamanders revealed that any other amphibian (Macgregor and del Pino, 1982).
the proportion of rDNA decreases with increasing DNA This fantastically great amount of rDNA presumably is
contení (Vlad, 1977). Furthermore, the total amount of capable of synthesizing far more RNA than mononu-
rDNA complementary to 18S and 28S rRNA is much cleate oocytes of most amphibians. Thus, it is expected
less in anurans than in salamanders, all of which have that the eggs of Flectonotus would be capable of syn-
much larger genome sizes than anurans. However, the thesizing much greater quantities of protein at a faster
interspecific variability in the proportion of the genome rate than other eggs. This may account for the rapid
that is complementary in sequence to 18S and 28S rRNA development of Flectonotus through a nonfeeding larval
suggests that factors oíher íhan the genome size may be stage.
significant in the franscription of RNA (see Vlad, 1977,
for review). Biochemical Genetics
The locaíion of RNA genes has been determined for Although genes are located on chromosomes and the loci
12 species of anurans and several species and subspecies for certain kinds of rDNA have been determined, among
of salamanders (see Batistoni et al., 1980; and Vitelli et amphibians as well as most other organisms, the genetic
al., 1982, for review). Of the salamanders that have been factors responsible for characters observed in the phe-
examined, there is variation in the sites of 18S + 28S notypes are mostly inferred, rather than known. Conse-
rDNA, and 5S DNA loci are found in different chromo- quently, the determinaüon of homogeneity and hetero-
somal positions. Among anurans, the 18S + 28S rRNA geneity at loci for a variety of genes coding for certain
genes are clustered in one locus per haploid chromosome proteins provides evidence for the genetic composition
sel; this locus is in an intercalary position proximal to the of organisms. Proteins subjected to electrophoresis can
centromere or cióse to the telomere. The 5S rRNA genes be identified chemically and different alíeles determined.
occur ai one to five loci per haploid complement. Each Estimates of genetic identíty (I) and genetic distance (D)
species has a distinctive pattern of 5S DNA loci, except between samples can be calculated by the methods of
that the two species of Xenopus studied have clusters of Nei (1972) and Rogers (1972) (but see Hillis, 1984, for
5S DNA near the telomeres of probably all chromo- correction of calculatíons). Molecular divergence also can
somes. Furthermore, in primitive salamanders and anu- be measured by immunological distance (ID) by means
rans having microchromosomes, 5S DNA loci are present of microcomplement fixatíon of serum albumins; one unit
on the microchromosomes, which do not have detectable of immunological distance is approximately equivalent to
loci for 18S + 28S DNA. In more advanced groups of a single amino acid difference between the samples com-
salamanders and anurans, microchromosomes are ab- pared (Maxson and A. Wilson, 1974).
sent, and the 5S DNA loci are present in the macrochro-
mosomes. This provides additional evidence for the Hybridization and Inheritance. Some of the earliest
incorporation of microchromosomes into the macrochro- work dealing with proteins concemed the identification
mosomes in the karyological evolution of amphibians. of hybrids with known or presumed parents (e.g., Gutt-
Gene amplification has been determined in various man's, 1972, work on Bufo). Utilization of numerous
mononucleate amphibians and in the multinucleate As- proteins has permitted the determination of natural hy-
caphus truei and Flectonotus pygmaeus (Macgregor and brids in numerous amphibians. Analysis of 30 proteins
Kezer, 1970; Macgregor and del Pino, 1982). Amplifi- of two species of hylid frogs, Pseudacrís nigrita and P.
cation is the multiplication of DNA sequences that code triseriata, in a narrow hybrid zone in the southem United
for 18S and 28S RNA (and the spacer sequences) within States revealed that 4 proteins showed different patterns
a nucleus to produce many copies of themselves that in parental and hybrid samples (Gartside, 1980). Like-
usually are not integrated physically into any chromo- wise, 4 of 26 proteins in the salamanders Desmognathus
some. The possession of large numbers of ribosomal genes fuscus and D. ochrophaeus reveal the occurrence of in-
and intense nucleolar actívity enables an oocyte to syn- terspecific hybridization in these species (Karlin and Gutt-
thesize as much RNA in a few months as would be pro- man, 1981). The European frogfíana esculenta is a hy-
duced by another kind of cell in several hundred years. bridogenetic hybrid of R. rídibunda and R. lessonae;
This RNA is incorporated into ribosomes that serve in examination of six loci showed no instance in which R.
protein synthesis from fertilization until feeding by the esculenta appeared to lack one of its alíeles derived from
hatchling. R. lessonae and the other from R. rídibunda (Uzzell and
Measurements of amounts of DNA per nucleus reveal Berger, 1975).
that in oocytes of Xenopus laeuis each nucleus produces In these and many other studies, the mode of inheri-
about 2000 copies of the genes for rDNA (Macgregor, tance of electrophoretic variants of proteins usually has
1968); approximately the same amount of replication is been inferred from the resemblance of protein pheno-
shared by eight nuclei in Ascaphus truei (Macgregor and types to patterns predicted by simple Mendelian inheri-
Kezer, 1970). However, each oocyte oí Flectonotus pyg- tance, by comparison with phenotypes for which the mode
maeus has in its early stages about 2500 nuclei, which of inheritance is known, or by studies of natural or labo-
EVOLUTION
456 Some genetic mutations in the Rana pipiens complex
crosses of the Australian tree frog Litaría ewingii dem- (Browder, 1975) and the R. escuíenta complex (Dubois,
onstrated that inheritance of transferrins is by a series of 1979c) involve color pattern (including albinism and mel-
at least nine codominant alíeles (Gartside and Watson, anism), as well as other kinds of recessive anomalies,
\y hybrids.
1976).Electrophoretic analysisis of
Only limited information laboratory
available concerning most of which are lethal. Albinism is a genetic recessive
the chromosomal loci for specific proteins. mutation in Xenopus laeuis (Hoperskaya, 1975). Color
Electrophoretic patterns of extracts of seven proteins mutants in laboratory-reared Ambystoma mexicanum
were examined with respect to the lampbrush chromo- provide an excellent opportunity for studying the nature
somes in oocytes of mature females produced ffom back- of gene actions that only now is being realized (S. Frost
crosses between female reciprocal hybrids oí Rana ni- and Malacinski, 1980).
gromaculata and R. brevipoda and males oímose parental
species (Nishioka et al., 1980). On the basis of the per- Ecológica! and Population Genetics. The prem-
centages of females whose genotypes agreed with a def- ises of ecological genetics are that natural populations are
inite bivalent chromosome, the loci of the genes con- adapted to their physical and biológica! environments and
trolling the proteins were determined. Linkage maps were that the genetic mechanisms respond to environmental
determined for R. clamitans (Elinson, 1983) and R. pi- change. There are many descriptive accounts of pheno-
piens (D. Wright et al., 1983). typic differences among species of amphibians in differ-
Laboratory production of interspecific hybrids of vari- ent environments, but the genetic factors responsible for
ous anurans has demonstrated differential genetic com- these differences are known in only a few cases.
patibility in reciprocal crosses and in backcrosses, as well The mottled "kandiyohi" and unspotted "burnsi" color
as different electrophoreüc patterns of proteins. Extensive morphs seem to have a selecüve advantage over the
experiments involving many species of Bufo (W. Blair, normal spotted morph of Rana pipiens in the north-cen-
1972; Kawamura et al, 1980), members of the North tral United States (Merrell, 1973). In the range of the
American Rana pipiens complex (J. Frost, 1982a; J. Frost unspotted morph, it and normal R. pipiens overwinter
and Platz, 1983), and Japanese ñaña (Kawamura and on the bottom of ponds. Comparisons of the numbers
Nishioka, 1978) have revealed chromosomal, electro- of individuáis of the two morphs in spring and fall show
phoretic, developmental, morphological, and vocaliza- that the unspotted morph has significantly higher survival
tíon differences between hybrids and parental species. during harsh winters, indicating that it has a physiological
Moreover, similar kinds of differences were found among adaptive advantage over the spotted morph and may be
parental species and their natural hybrids in North Amer- maintained by a form of seasonal selection. The mottled
ican hylids—e.g., Pseudacñs (Gartside, 1980) and Hy/a and spotted morphs occur sympatrically in prairie habi-
(H. Gerhardt et al., 1980). tats, where tadpoles of the mottled morph metamor-
Anurans have proved to be especially useful in hy- phose significantly sooner than those of the spotted morph.
bridizatíon studies because many species that have ex- Thus, the mottled morph presumably is maintained
ternal fertilizaüon of aquatic eggs can be crossed ¡n the through selective advantage of more rapid larval devel-
laboratory. The results of such crosses have provided opment in prairie ponds that are subject to desiccatíon.
information about the degrees of genetic compatibility Geographic variation in proteins has been demon-
and are beginning to provide data on genetic markers strated in several species of amphibians. These patterns
that will permit the chromosomal localization of loci for have been interpreted in three ways: (1) If the majority
certain genes (D. Wright et al., 1983). of electrophoretic variation is physiologically irrelevant.
Hybridizatíon experiments have provided evidence for the geographic patterns may be the result of genetic drift
the inheritance of certain color pattern traits. In fíana and gene flow among populations. (2) Different allo-
pipiens the mottled "kandiyohi" and unspotted "burnsi" zymes at each locus are adapted to local environments
variants are expressed by two dominant nonallelic genes and respond to selection. (3) The electrophoretic variants
(Volpe, 1961); furthermore, the unspotted variant is a are physiologically neutral but are linked to loci that are
manifestation of genic interacüon between a major pig- under the influence of selection. In the newt, Noto-
mentary locus and a complex of modifying "minor-spot- phthalmus virídescens, four of five loci examined showed
tíng" genes (Volpe and Dasgupta, 1962). correlations with environmental parameters (Tabachnick,
Comparison of crosses with Mendelian expectations 1977). Genetic variation is very high in Bu/o uiridis; 9-16
indicates that the presence of a middorsal stripe in Acris of 26 loci are polymorphic among populations of this
crepitans is dominant in a single alíele (Pyburn, 1961). toad in Israel (Dessauer et al., 1975). Frequencies of two
In fact, in various kinds of amphibians that have pattern alíeles undergo clinal shifts corresponding to the rainfall
dimorphism of striped versus nonstriped individuáis, the gradient. The degree of isolation of populations of B.
gene for the striped pattern is dominant—e.g., Plethodon uiridis in the Negev and Sinai deserts results in only slightly
cinéreas (Highton, 1959), Discoghssus pictus (Lantz, less polymorphism, but a population on Vis Island, in the
1947), Eleutherodactylus planirostrís and some Jamaican Adriatic Sea, has low heterozygosity. As a rule, island
species of Eleutherodactylus (Goin, 1947, 1950), and populations may be less polymorphic than mainland
ffana /¡mnocharis (Moriwaki, 1953). populations, as is evident in B. americanus on islands in
 Cytogenetic, Molecular, and Genomic Evolution
Lake Michigan (Abramoff et al., 1964). Only 5 of 27 loci 1980) and Plethodon (Highton and Larson, 1979), and 457
are monomorphic in Hy/a arbórea in Israel. The spatíal for various anuran taxa, the most extensive being the
patterns and environmental correlates and predictors of determination of genetic relationships on the basis of 50
genic variation in this species suggest that protein poly- loci among 20 species of the Rana pipiens complex (Hillis
morphisms are largely adaptive and are molded primarily et al., 1983). Likewise, relationships of taxa have been
by climatic selection rather than by stochastic processes hypothesized by immunological distances determined by
or neutrality (Nevo and Yang, 1979). In contrast, only 1 microcomplement fixation of serum albumins. In this
of 32 loci is polymorphic in each of two species of Pe- manner, relationships have been postulated among such
lobates. These extremely homozygous species are fos- diverse groups as Leiopelma (Daugherty et al., 1981),
sorial, like other organisms displaying very low hetero- Xenopus (Bisbee et al., 1977), myobatrachines (Daugh-
zygosity, which seems to be the result of selection by erty and Maxson, 1982), African and Eurasian Bu/o
constant environments (Nevo, 1976). (Maxson, 1981a, 1981b), and South American frogs of
The degree of relative heterogeneity in local popula- the genera Leptodacíy/us (Heyer and Maxson, 1982) and
tions (and the rate and amount of local differentiation) Gastrotheca (Scanlan et al., 1980). The same techniques
can be affected by the form of the postmetamorphic range have been applied to plethodontid salamanders (Maxson
(continuous, fragmented, linear, ortwo-dimensional), the et al., 1979; Maxson and D. Wake, 1981) and caecilians
relationship of the nonbreeding range to the breeding (Case and M. Wake, 1977).
site, and the tendency to form breeding aggregations. Both electrophoretic analysis of proteins and micro-
Electrophoretic data on seven species of anurans in Ma- complement fixation of serum albumins have provided
laysia indícate that those species that have the most re- congruent results in North American Hy/a (Maxson and
stricted ranges and do not aggregate for breeding have A. Wilson, 1975; Case et al., 1975) and fíana (Case,
the greatest homogeneity, whereas those with two-di- 1978), and in European and Californian species of sal-
mensional ranges and that aggregate for breeding (thereby amanders of the genus Hydromantes (D. Wake et al.,
resulting in the most interbreeding of individuáis from 1978). The most thorough analyses of genetic relation-
throughout a large, local range) have the greatest het- ships have been with the genus Plethodon, in which re-
erogeneity (Inger et al., 1974). sults of electrophoretic analyses of 29 loci (Highton and
In a review of the amounts of protein heterogeneity in Larson, 1979), immunological distances (Maxson et al.,
animáis, Nevo (1978) noted the high heterogeneity in 1979), and DNA hybridizatíon (Mizuno and Macgregor,
lowland tropical anurans, as compared with températe 1974) yielded cióse comparisons (Maxson and Maxson,
species. As a rule, anurans in the lowland humid tropics 1979). For the most part the biochemical data are highly
breed frequently, whereas those in the températe regions congruent with morphological variation (Larson et al.,
usually breed only once or twice per year. Consequently, 1981).
in tropical species there is more opportunity for genetic In several groups that have been studied, there are
interchange among individuáis in a given population and striking differences between the rates of molecular and
an expected higher amount of heterogeneity. morphological evolution. Measurements of molecular ev-
olutíon are strictly estimations of divergence, whereas
Speciation and Phylogenetics. The determination morphological convergence can give a false impression
of genetic differences between species by electrophoretic of relationships. Conversely, morphological divergence
assays of proteins has provided a new dimensión to sys- might be a rapid phenomenon in response to adaptive
tematics. Electrophoretic studies on salamanders of the shifts, while molecular evolution proceeds at an appar-
genera Desmognathus (Tilley et al., 1978; Tilley and ently constant rate. Thus, the Middle American hylid frog
Schwerdtfeger, 1981), Taricha (Hedgecock, 1976), Tri- Anotheca spinosa is much closer to hylines immunolog-
turas (Kalezic and Hedgecock, 1980), and Ambystoma ically than it is to the more morphologically similar hemi-
(Pierce and Mitton, 1980), among others, have provided phractines, and is an example of morphological conver-
biochemical data in support of morphological characters gence (Maxson, 1977). Some morphological similarities
for the recognition of species. Likewise, similar studies in populations of Aneides flavipunctatus are the result of
on North American Scaphiopus (Sattler, 1980), Rana (Post independen! paedomorphic changes, whereas protein di-
and Uzzell, 1981), and Hy/a (Case et al., 1975) and on vergence has been constant (Larson, 1980). Entering new
Papuan Litaría (Dessauer et al., 1977) have supported adaptive zones may re§ult-in highly distinctive morpho-
previous systematic arrangements and, in some cases, logical divergence that belies the genetic similarities. For
have pointed out the existence of previously unknown example, the semiaquatic hylid frogs of the genus Acris
differentiation. Assays of láclate dehydrogenase provided are highly diverg^nt morphologically from other North
interfamilial comparisons of salamanders (Salthe and American hylids; however, immunologically they are no
Kaplan, 1966). more divergen! than various groups of species of North
The phylogenetic relationships among taxa have been American Hy/a (Maxson and A. Wilson, 1975). Likewise,
hypothesized by measures of genetic distances of pro- arboreal salamanders of the genus Aneides have a dis-
teins based on electrophoretic data for a variety of tinctive suite of morphological characters, but biochem-
plethodontid salamanders, notably Batmchoseps (Yanev, ically they are more closely related to species of Pletho-
EVOLUTION
458 c¡on ¡n western North America than the latter are to their recent divergence of the species living in high montane
eastern congeners (Larson et al., 1981). Some adaptive environments that did not exist prior to the end of the
shifts in reproductive modes are relatively recent; for ex- Pliocene (Scanlan et al., 1980).
\, some species of Anjean marsupial frogs (Gastro- Among the salamanders, the time of divergence of lin-
theca) that have eggs tha/ hatch as tadpoles are immu- eages of Hydromantes, as based on molecular analyses,
nologically closer to species that have eggs that undergo corresponds well with the severance of the land connec-
direct development than they are to other tadpole-pro- tions between North America and Europe (D. Wake et
ducing species (Scanlan et al., 1980). Although Rheo- al., 1978); however, the timing of divergence of holarctic
batrachus has a unique reproductive mode, its biochem- pelobatid frogs seems to have been much earlier (Sage
ical divergence is about the same as various other genera et al., 1982). Also, the time of divergence of eastern and
of myobatrachids that have generalized reproductive western species groups of Plethodon corresponds with
modes (Daugherty and Maxson, 1982). the discontinuity of forests across North America (High-
ton and Larson, 1979; Maxson et al., 1979). The pattern
Temporal Evolution. Subsequent to the discovery of speciation and distribution of salamanders of the genus
that albumin evolution proceeds in a clocklike fashion Batrachoseps in California can be superimposed on a
(Sarich and A. Wilson, 1967), there has been a rapidly time-series of reconstructions of geological, climatic, and
growing body of evidence that protein evolution pro- botanical history of the área for the past 10 million years
ceeds at an approximately constant rate and that the (Yanev, 1980). The genetic distance between some Cen-
comparison of this rate with fossils of a known age and tral and South American species of Boütoghssa provides
dated geological events provides a sound basis for dating estímales of divergence time up to 18 million years ago,
the sequenüal times of divergences of lineages of living about 11 million years before the earliest estimated clo-
organisms (see A. Wilson et al., 1977, for review and sure of the Panamanian Portal and the establishment of
Throckmorton et al., 1978, for application to phyloge- a continuous land connection between the American
netics). Although controversy has arisen (see Korey, 1981), continents; thus, the divergence times are either grossly
the evidence seems to favor the regularity of evolutionary overestimated or a bolitoglossine salamander crossed the
rates of homologous molecules; the discrepancies com- water gap and entered South America in the Pliocene
monly noted between divergence times calculated on im- (Hanken and D. Wake, 1982).
munological distances (ID) and those on Nei distances
(D) may be because neither (ID ñor D) is in fact an ac-
curate measure of time. Electrophoretic Nei distances are GENOMIC EVOLUTION
most sensitive for comparison of recently diverged pro- Morescalchi (1977, 1979, 1980) and Birstein (1982) re-
teins, and because albumin comparison encompasses a viewed evidence for evolution of karyotypes in amphib-
much greater range of phyletic distances, the measure of ians; Morescalchi generalized that in all three living groups
immunological distance is an excellent method for de- there are trends toward (1) a restricted number of chro-
termining evolutionary relationships and divergence times mosomes (all metacentric and differing little in size), (2)
(Maxson and Maxson, 1979); 100 unitsof immunological an increase in the amount of nuclear DNA, especially in
distance accumulate every 55-60 million years of lineage salamanders, and (3) striking interspecific variability in
separation in amphibians (Carlson et al., 1978). genome size, even among related species having mor-
Dating of temporal sequences of molecular divergence phologically similar karyotypes.
in various groups of amphibians for the most part has Cytogeneticists have argued that centromeres may be
been consistent with the dating of geological events and/ lost but not gained, so karyotypic evolution has involved
or paleoclimatic changes that presumably were important the incorporation of genetic material from a large number
to the diversification of sepárate phyletic lineages. Thus, of telocentric chromosomes into a smaller number of
the divergence of two lineages of egg-brooding hylid frogs, metacentric chromosomes, a general trend apparent in
Cryptobatrachus and Stefania, in South America having amphibians. However, recent cytogenetic evidence sug-
an immunological distance of 155 units is timed to have gests that centromeres may be gained and that telomeres
occurred in the Middle Cretaceous, the time of uplift of may function as centromeres following chromosomal fis-
the Guianan Highlands, an área where Stefania is en- sion (Holmquist and Dañéis, 1979). Multiplication of
demic (Duellman and Hoogmoed, 1984). The antiquity chromosomes by centric fission or centromeric dissocia-
of generic lineages of leptodactylid frogs inhabiting the tion presumably has occurred in several groups of frogs.
ancient Brazilian Shield contrasts with the recent diver- especially Eleutherodacfylus and some neotropical hylid
gence times of species in lineages inhabiting the young frogs. Possibly this chromosomal rearrangement is sig-
Andes (Maxson and Heyer, 1982). The timing of the nificant in the rapid speciation in these groups. In contrast
uplift of different parts of the Andes in the Cenozoic and to salamanders, polyploidy is fairly common in anurans:
Quaternary corresponds to the times of divergence among this is another way to increase not only genetic hetero-
lineages of lowland species of marsupial frogs (Gasíro- geneity but also genome size.
theca) on either side of the Andes and of the much more Superimposed on the general trends are other devia-
 Cytogenetic, Molecular, and Genomic Evolution
tions, at least some of which seem to be highly adaptive. al., 1977; among others) that molecular evolution is cor- 459
One of these deviations is the independent increasc to related more highly with karyotypic evolution than with
very high levéis of nuclear DNA in families of neotenic structural gene evolution have resulted in more attenüon
salamanders. At the cellular level these increases in nu- to changes in karyotypes by evolutionary biologists. Sta-
clear DNA seem to parallel increases in nuclear and cel- tistically significant correlations between estímales of ge-
lular volumes and in cell surface áreas; these increases netic distance based on albumins, múltiple proteins, and
result in an inverse ratio of cell surface to cell volume, hybridization of nonrepetitive DNA in plethodontid sal-
which can be considered as an Índex of the rate of oxi- amanders (Maxson and Maxson, 1979) provided the
datíve metabolism. Lacking physiological mechanisms molecular basis for comparisons of rates of molecular and
capable of controlling the rate of oxidative metabolism in chromosomal evolution in salamanders (Maxson and A.
the organism as a whole, possibly amphibians exercise Wilson, 1979). Gross comparisons between estimated time
this control at least parüally at the cellular level, the modes of divergence (based on immunological distances) and
and amounts depending on the adaptive strategies of the pairs of species having the same karyotype provided an
species. The genome size is implicated in these phenom- estímate of 0.006 point mutation per lineage per million
ena, but it is not clear whether the variations in the total years, a rate about half that estimated for anurans. The
amount of nuclear DNA are the cause or only the effects major difference is between amphibians and mammals;
of the interspecific differences in the relatíve cell surfaces by comparison with amphibians, mammals have greatly
and therefore of general metabolism. diversified karyologically in a much shorter period of time.
Considerable amounts of data support the hypothesis Thus, the conservativeness of the amphibian karyotype
that there is a positive correlation between the total amount is evident. However, only gross morphology of the chro-
of nuclear DNA and duration of development. However, mosomes has been considered. These karyotypic simi-
limited data suggest that increases in certain sequences larities may mask possible substructural differences that
of DNA might enhance the rate of development by more are being discovered in amphibian chromosomes. The
effective protein synthesis. Therefore, it is possible that answers to the relationships of molecular and karyotypic
some of the variations observed in developmental rates evolution lie in the determination of the positions of the
are influenced not only by the quantity, but more spe- loci for the various genes.
cifically by the quality, of the nuclear DNA. These differ- Finally, as emphasized by D. Wake (1981), molecular
ences, like those in genome size with respect to cellular techniques have become an important new componen!
volume and surface, must be viewed as adaptive varia- in systematics, which traditíonally has been based mostly
tions that have evolved separately in different lineages on morphological data. The integration of molecular and
and that are independent of the major evolutionary trends traditional approaches greatly increases the potential for
in the three orders of amphibians. generating and testing hypotheses of phylogenetic rela-
Recent suggestíons (A. Wilson et al., 1974; Bush et tionships and temporal evolution of lineages.
 CHAPTER 17
¡fwe are lo compare partera with theories
ofprocess—as we musí do to improve our
very notions ofprocess—we must have ai
the very least an accurate concept of
evolutionary genealogy.
Niles Eldredge andJoel Cracraft (1980) Phylogeoy

T
1 HE . he evolutionary or phylogenetic relationships among
the families of living amphibians are basic to an interpre-
the WAGNER78 computer program written by J. S. Far-
ris. Depending on the number of convergences or re-
tation of their biogeography and to constructing a mean- versáis (homoplasies), alternativo phylogenetic trees (cla-
ingful classification. Thus, the material presented in this dograms) were generated. The preferred arrangement is
chapter is fundamental to the biogeographic synthesis the most parsimonious cladogram, that is, the one having
(Chapter 18) and the classification of the modern groups the highest consistency Índex (minimal number of pos-
of amphibians (Chapter 19). sible changes in character states/actual number of changes).
With the development of testable hypotheses of phy- For each of the living orders of amphibians, the trans-
logenetic relationships based on shared derived character formation series used in a phylogenetic reconstruction at
states as proposed by Hennig (see E. Wiley, 1981, for a the family level are described and their characters noted
recent synthesis), systematists have an explicit and ob- as primitive (0) or derived (1). In all cases the direction
jectíve methodology for determining phylogenetic rela- of evolutionary change is O —» 1. In those cases in which
tionships. This system is based on the identification of there is more than one derived character, the characters
homologous structures and evolutionary direction (po- are derived sequentially or serially (i.e., O —> 1 —> 2, etc.)
larity) of transformation series from a primitive character unless it is specified that certain characters are derived
(plesiomorphy) to a derived character. A theory of phy- independently (i.e., l'«— O —> 1 —» 2). The direction (po-
logenetic relationships is based on nested sets of derived larity) of evolutionary change is determined by the char-
character states (apomorphies) shared by two or more acters in an outgroup. For most characters the outgroup
lineages, whereas primitive characters (plesiomorphies) is other lissamphibians or tetrapods.
shared by two or more taxa do not show relationships.
Characters that are unique to a given lineage (autapo-
morphies) are useful in recognizing a particular lineage CAUDATA
but not in determining the relationship of that lineage
with any other one. Character States
In the following analyses of phylogenetic relationships The states of 30 characters that are variable within the
among the living groups of amphibians, hypothesized families of salamanders are described below. The distri-
phylogenetic relationships were reconstructed by using butíon of character states is given in Table 17-1. An ad-

461
EVOLUTION
462 Table 17-1. Distribution of Character States in Families of Salamanders"

Living families Extinct families

i 1

Cryptobrancl

Scapherpeto
Amphiamida

Batrachosau

Karanridae
Hynobiidae
•

Sirenidae
1

Characterb
| J
Q
j
A. Fusión of premaxillae 0 1 0 0 0 oc 0 Oc 0 0 0 0 0
B. Dorsal process of premaxilla 1 1 0 1 0 1 1 1 0 1 0 1 1
C. Maxilla 0 0 0 0 0 Oc 1 0 1/1' 0 0 0 0
D. Septomaxilla 0 1 1 0 0 Oc 1 1 1 9 9 9 9
E. Nasal ossificatíon r r 0 l' d 0 1' 1" 1' r 9 9 9 9
F. Lacrimal i i 1 0 0 1 1 1 i 9 0 0 9
G. Quadratojugal i i 1 1 1 1 1 1 i 1 0 1 1
H. Otic-occipital ossificatíon i i 0 0 0 1 0 1 0 1 0 1 0
I. Pterygoid 0 i 0 od 0 2 0 0 i 0 0 0 0
J. Intemal carotíd foramen (y 0 1 0 1 1 0 1 i 1 0 1 1
K. Opercular apparatus i i 0 0 0 2 0 1 0 9 0 9 9
L. Junction of periotic canal and 2 2 1 2 2 2 1 2 0 9 9 9 9
cistern
M. Flexures of periotic canal 1 1 1 ld 1 2" 1 2e 0 9 9 9 9
N. Basilaris complex of inner ear 0 0 0 0 0 2 2 0° 2 9 9 9 9
0. Angular 1 1 0 1 0 1 1 1 1 0 0 0 0
P. First hypobranchial and first 0 0 1 0 1 0 0 Oc 0 9 9 9 9
ceratobranchial
Q. Second ceratobranchial 1 1 0 1 0 1 1 1 1 0 0 0 0
R. Number of larval gilí slits 0 1 0 0 0 0/1 2 0 1/3 9 9 9 9
S. Palatal dentitíon 0 1 1 1"" 0 1" 1 r 1'" 9 1 9 1
T. Tooth structure 0 0 0 0 0 0 0 0 1 0 0 1 0
U. Scapulocoracoid 1 1 1 1 1 1 1 i 0 1 1 1 1
V. Vertebrae 0 0 0 0 0 r 0 i 0 0/1 0 0 0
W. Ribs 0 0 1 0 1 0 0 0 0 0 0 0 0
X. Spinal nerves 3 1 0 2 0 3 0 4 4 0 0 0 2
Y. Ypsiloid cartilage 0 1 0 0 0 1 1 0 1 9 9 9 9
Z. Levator mandibulae muscle 1' r r r r r 1' r 1 1' 0 1' r
AA. Pubotibialis and puboischiotibialis 0 0 i 0 i 0 0 0 0 0 0 0 0
muscles
BB. Kidney 1 i i i i i 1 i 0 9 9 9 9
CC. Mode of fertilization 1 i 0 i 0 i 1 i 0 9 9 9 9
DD. Chromosomes 3 2 0 3 0 3 1 2 4 9 9 9 9

°0 = primitive; 1, 2, etc. = derived; ? = unknown. Autapomorphies not included.

6See text for definitíons of states.
cDerived state in some taxa.
dRhyacotriton differs: E = 1", I = 1, M = 2.
eNext most derived state in some taxa.

ditíonal 10 autapomorphic characters are listed and their B. Dorsal Process of Premaxilla.—In primitive tetra-
unique taxa identified; these characters are not listed in pods and porolepiform fishes, the dorsal processes of the
Table 17-1. premaxillae do not sepárate the nasals; these processes
A. Fusión of Premaxillae.—Primitively in tetrapods, extend posteriorly and sepárate the nasals in some fam-
the premaxillary bones are paired. Two premaxillae are ilies of salamanders. Short dorsal processes are consid-
considered to be primitive (0) and fused premaxillae de- ered to be primitive (0) and long processes separating
rived (1). Fusión of the premaxillae is an ontogenetic the nasals derived (1).
phenomenon in some hynobiids and salamandrids, and C. Maxilla.—Maxillary bones are present in most
in most plethodontids, although in some of the latter the gnathostomes. Presence of maxillae ¡s primitive (0). Their
premaxillae are fused in larvae (D. Wake, 1966). Thus, loss is derived (1) independently in the Proteidae and in
the derived state has evolved independently in each of the paedomorphic Pseudobranchus (Sirenidae) and in
these families, and in the Amphiumidae, which paedo- Haideotriton, Typhlomolge, and some Eurycea and Gyr-
morphically retains the conditíon in adults. ¡nophi/us (Plethodontidae). Maxillae are the last dentig-
 Phylogeny
erous bones to ossify during ontogeny, and in many neo- and its funcüonal replacement by the footplate of the 463
tenic salamanders the maxillae are small. Therefore, columella (2) (Monath, 1965; Larsen, 1963).
absence of maxillae is a paedomorphic condition (Lar- L. Junction of Períotic Canal and Cistern.—In the
sen, 1963). The absence of teeth on the maxillae (state inner ear, the periotic canal joins the periotic cistern dor-
1') is an independently derived state from the primitive sally at its posterior aspect in caecilians, anurans, and
condition and in sirenids is correlated with the presence some salamanders; Lombard (1977) considered this to
of a horny beak (see Character EE). be the primitive state (0). Two sequentially derived states
D. Septomaxilla.—The small, paired septomaxillary are the junction of the canal with the cistern slightly dorsal
bones associated with the nasal capsules are present and posterior to the fenestra ovalis (1), and junction of
primitively in tetrapods, but they are absent in several the canal by a protrusion of the cistern into the fenestra
groups of salamanders, including all of the oblígate neo- ovalis (2). Most salamanders have state 2, but some ob-
tenes. In salamanders that metamorphose, the septo- lígate neotenes and larvae of dicamptodonüds and am-
maxillae are formed late in ontogeny. The presence of bystomatids have state 1 (Lombard, 1977).
septomaxillae is considered to be primitive (0), and the M. Flexures of Periotic Canal.—In the inner ear, the
paedomorphic loss of these elements is derived (1). Among periotic canal curves ventrally and medially from its junc-
the plethodontids, the derived state is found in the neo- tion with the periotic cistern in caecilians, anurans, and
tenic Haideotríton, Typhlomolge, and Gyrinophi/us pal- some salamanders. This is considered to be the primitive
leucus, in the paedomorphic species of Eurycea, and in state in salamanders (0). A derived state is a relatively
some bolitoglossines (D. Wake, 1966). horizontal course of the canal (1). Lombard (1977) rec-
E. Nasal Ossification.—In some salamanders and all ognized four modifications of this derived state but could
other living lissamphibians, the nasals ossify from two not demónstrate polarities convincingly, so only one sec-
cartilaginous anlagen (Jurgens, 1971). This is considered ondarily derived state is recognized here—canal with one
to be the primitive condition in salamanders (0). Inde- or more flexures (2). Reversáis from state 2 to state 1
pendently derived states include ossification from only apparently have occurred in Notophthalmus (Salaman-
the median anlage (1), from only the lateral anlage (!'), dridae) and in Batrachoseps and Thorius (Plethodonti-
or reducüon or absence (1") in Rhyacotriton (Dicamp- dae).
todontidae), proteids, and some bolitoglossine pletho- N. Basilaris Complex of Inner Ear.—In anurans,
dontids (Nototriton and Thorius). primitive caecilians, and some salamanders, a recessus
F. Lacrimal.—Primitively, a lacrimal bone is present basilaris and papillae are present in the inner ear (0).
in the facial región of tetrapods. In salamanders, the pres- Lombard (1977) indicated that sequentially derived states
ence of a lacrimal is considered to be primitive (0), and are the absence of papillae (1) and the absence of the
the loss of the bone is derived (1). entire complex (2). Some derived genera of salamandrids
G. Quadratojugal.—Primitively in most tetrapods, this have state 1 or 2; state 1 is not characteristic of any family
element is present in the maxillary arch. Its presence is of salamanders.
considered to be primitive (0) and its absence derived O. Angular.—Primitively in tetrapods, an angular bone
(1). is present as a sepárate element in the lower jaw. In
H. Otic-Occipital Ossification.—Primitively in tetra- salamanders, the presence of a sepárate angular is con-
pods, the exoccipital, prootic, and opisthotic are sepárate sidered to be primitive (0); its fusión with the prearticular
elements. This is considered to be the primitive state in is derived (1).
salamanders (0), whereas the fusión of these elements P. First Hypobranchial and First Ceratobran-
into a single otic-occipital element is derived (1). chial.—In most lissamphibians (at least larval forms), the
I. Pterygoid.—Paired pterygoid bones form part of first hypobranchial and first ceratobranchial (ceratobran-
the palate in primitive tetrapods. The presence of these chial and epibranchial, respectively, of some authors) in
elements is considered to be primitive (0), whereas se- the hyoid arch are sepárate elements. This is considered
quenüally derived states are reduction (1) and absence to be the primitive state (0). The fusión of these two
(2). elements into a single cartilaginous rod is derived (1).
J. Infernal Carotid Foramen.—Primitively in tetra- Q. Second Ceratobranchial.—The second cerato-
pods, an internal carotid foramen is present in the lateral branchial (epibranchial of some authors) persists in adults
alae of the parasphenoid. This is considered to be the of primitive tetrapods. This is considered to be the prim-
primitive state in salamanders (0); the absence of the itive state (0). The loss of the second ceratobranchial
foramen is derived (1). during metamorphosis is derived (1).
K. Opercular Apparatus.—Primitively in tetrapods, R. Number of Larval Gilí Slits.—Four pairs of gilí
the opercular apparatus consists of an ossified operculum slits are present in various primitive tetrapods and in most
and free, ossified columella; this is considered to be the salamanders. This is the primitive state (0). In various
primitive state in salamanders (0). A derived state is the neotenic salamanders, the number of gilí slits is reduced;
fusión of the columella with the operculum (1); a sec- these presumably serially derived states are three pairs
ondarily derived state is the loss of the original operculum (1), two pairs (2), or one pair (3). Within the Sirenidae,
EVOLUTION
464 two states are present—three pairs in Siren and one in manders (0). Independently derived states are an origin
Pseudobranchus; among plethodonüds, the desmogna- on the side of the skull (1) or an origin that includes the
thines have four pairs, and the others have three. On- exoccipital (and, in some cases, the cervical vertebrae)
togenetic reduction in the number of slits occurs in cryp- U').
tobranchids and amphiumids. AA. Pubotibialis and Puboischiotibialis Muscles.—
S. Palatal Dentition.—Based on larval and adult These thigh muscles are sepárate in anurans and some
dentíüon patterns, Regal (1966) concluded that the pat- salamanders. This is considered to be the primitive con-
tern of transverse palatal dentiüon was primitive (0). Five dition (0), whereas the fusión of the two muscles is de-
states seem to be derived independently—teeth parallel rived (1).
to premaxillary and maxillary teeth (1), longitudinal ex- BB. Kidney.—Glomeruli normally are well developed
tensions of teeth along the lateral edges of the vomers anteriorly in the kidney in lissamphibians. This might be
(!'), longitudinal extensions of teeth along the medial considered the primitive state (0); reduction or absence
edges of the vomers (1"), teeth in large patches (!"'), and of anterior glomeruli is the derived state (1).
teeth in M-shaped pattern (!"")• CC. Mode of Fertilization.—Extemal fertilizatíon is the
T. Tooth Structure.—Primitívely, tetrapods have un- primitive state in tetrapods (0). Modified cloacal glands
divided teeth, whereas teeth that are divided into a dis- for the production of spermatophores and the presence
tinct crown and pedicel are characteristic of most lissam- of a spermatheca in females are derived characters for
phibians (Parsons a^d Williams, 1962). Within the internal fertilization in salamanders (1).
Lissamphibia, pedicellate teeth must be considered as the DD. Chromosomes.—In primitive groups of the three
primitive state (0), and the presence of undivided teeth living orders of amphibians, there is a large number of
is viewed as derived (1), either as a paedomorphic state chromosomes that includes many microchromosomes.
or as a character reversal. An intermedíate condition, The presence of microchromosomes that constitute a dis-
termed subpedicellate by Estes (1981), occurs in the Ba- tinct size class from the macrochromosomes, and of a
trachosauroididae and Proteidae. diploid number of 56 or more chromosomes ¡s consid-
U. Scapulocoracoid.—Primitívely in tetrapods, a ered to be primitive (0). Sequentially derived states are:
sepárate /coracoid bone is present in the pectoral girdle; diploid number of 38 chromosomes ¡ncluding one pair
this con'ditíon is considered to be primitive (0), whereas of microchromosomes (1), diploid number of 22 to 28
the absence of a sepárate coracoid center of ossification macrochromosomes gradually decreasing in size to mi-
is derived (1). crochromosomes (2), diploid number of 26 or 28 ma-
V. Vertebrae.—Primitívely among tetrapods, the am- crochromosomes with no microchromosomes (3). An
phicoelous condition of vertebral centra is considered to independently derived state is 46 to 64 macrochromo-
be primitive (0). According to D. Wake and Lawson (1973), somes and no microchromosomes (!'). See Table 16-2
opisthocoely is derived in different ways in the Salaman- for chromosome numbers.
dridae (1) and Plethodontidae (!').
W. Ribs.—Primitívely in many tetrapods, the ribs are Autapomorphies. Although they are not useful in de-
bicapitate. This is the primitive condition in salamanders termining relationships, uniquely derived character states
(0); unicapitate ribs are derived (1). are helpful in diagnosing some families.
X. Spinal Nenes.—All spinal nerves exit interverte- EE. Premaxillary Dentition.—The pars dentalis of the
brally from the vertebral column in primitive tetrapods premaxilla bears teeth in primitive tetrapods, but it is re-
(except the limbless aistopods). This is considered to be duced in size and edentate in sirenids. Presence of pre-
the primitive state in salamanders (0). Edwards (1976) maxillary teeth is considered to be primitive (0) and ab-
defined several derived states in salamanders: only the sence of teeth derived (1). In sirenids, a homy beak covers
posterior caudal nerves exiting through foramina in the the premaxillae and maxillae, which also are edentate;
vertebra (1), all postsacral nerves exiting intravertebrally the presence of a horny beak is correlated absolutely with
(2), all but the first three nerves exiting intravertebrally the absence of teeth and is not considered to be a sep-
(3), and all but the first two nerves exiting intravertebrally árate character. The presence of a horny beak in place
(4). These character states are derived sequentially. of teeth is an autapomorphy for sirenids.
Y. Ypsiloid Cartilage.—The ypsiloid cartilage, at- FF. Frontal.—Tríese roofing bones normally are paired
tached to an anterior process of the pubis, is associated (0); they are fused into a single element (1) in the Pro-
with the presence of lungs in terrestrial salamanders, and sirenidae (Estes, 1981).
it is absent in plethodontids and several neotenic groups. GG. Fronto-squamosal Arch.—Primitive salaman-
Presence of the cartilage is primitive (0), and its absence ders lack an arch (0), which is present only in salaman-
is derived (1). drids as a derived state (1). The arch is reduced or absent
Z. Levator Mandibulae Muscle.—The m. levator in some salamandrids; these are considered by D. Wake
(= adductor) mandibulae anterior (= internus) superfi- and Ozeti (1969) to be secondarily derived states in that
cialis originales on the skull roof in early tetrapods. Estes family.
(1981) considered this to be the primitive state in sala- HH. Mandibular Symphysis.—The unión of the
 Phylogeny
mandibular rami is simple in most salamanders (0), but K, 0-Q, T, U, W, X, Z, AA-GG, KK-NN); 465
the rami have an interlocking symphysis (1) in prosiren- consistency índex = 73%.
ids. 5. All families using 20 characters (those that are
II. Atlas-Axis Complex.—In most amphibians the not strongly paedomorphic and for which data
cervical vertebrae are unmodified (0), but these vertebrae are available for extinct families—A-C, G, H,
are modified to form an analogue of the atlas-axis com- O, Q, T, U, W, X, Z, AA, EE-KK); consistency
plex (1) in the Prosirenidae (Estes, 1981). índex = 72.5%.
JJ. Tubercu/um Interglenoideum.—An intercotylar
process, the tuberculum interglenoideum, is present on In the cladogram based on 37 characters of Recent
the atlas of most salamanders. Estes (1981) considered families, the paedomorphic families Amphiumidae, Pro-
this to be the primitive state (0) and the absence of the teidae, and Sirenidae are clustered. In all of the other
process in batrachosauroidids to be derived (1). analyses, except the one of non-paedomorphic charac-
KK. Pelvic Gírale.—A pelvic girdle and hindlimbs are ters of Recent families, the Salamandridae and Sirenidae
normal tetrapod characters (0). The loss of these struc- share a stem. One shared derived state (Character X—
tures in several groups of vertebrates, including sirenid all but the first two spinal nerves exiting intravertebrally)
salamanders, is an independently derived state (1). is responsible for this arrangement. Elimination of that
LL. Nasolabial Groove.—The nasolabial región in most character results in shifting the Sirenidae to a posítion
living amphibians lacks grooves (0); these sensory struc- between the Karauridae and the stem leading to all other
tures are derived in plethodontids (1). líving salamanders.
MM. Lungs.—Lungs typically are present in meta- In all cladograms, the Cryptobranchidae and Hyno-
morphosed salamanders (0); their absence in plethodon- biidae have a common stem, and the Ambystomatidae,
tids and Onyc/iodacty/us (Hynobiidae) is independently Salamandridae, and Plethodontidae have a common stem.
derived (1). Lungs are reduced in Rhyacotriton, Rano- In those cladograms including extinct families, the Sca-
don, and several genera of salamandrids. pherpetontidae and Dicamptodontidae and the Batra-
NN. Interventricular Septum.—The ventricle typi- chosauroididae and Prosirenidae are clustered, and the
cally is a single chamber in primitive tetrapods (0), in- Karauridae is always primitive. Depending on the cla-
cluding all amphibians; an interventricular septum is present dogram, the positions of the Amphiumidae, Dicampto-
(1) in sirenids (J. Putnam, 1975). dontidae, and Proteidae change with respect to one an-
other.
The placement of the Sirenidae is a major problem.
Phylogeny Depending on the character set used, sirenids have 3-5
The major problem in reconstructing a phylogeny of sal- character reversáis and 1-4 character convergences, plus
amanders is the large number of paedomorphic charac- a suite of seven autapomorphies. Obviously, sirenids have
ters that result in similar character states in adults of some a peculiar combination of primitive and derived character
families and in larvae of presumed more primitive groups. states, not all of which are associated with paedomor-
Moreover, many of the characters are unknown in the phosis.
extinct families; the characters of these and Recent groups The preferred cladogram of Recent families is one in
have been reviewed most recently by Estes (1981). Hecht which strongly paedomorphic characters are excluded.
and Edwards (1977) discussed the familial characters of This cladogram based on these 27 characters can be
salamanders in relation to their phylogeny. In the most modified by assuming the states of some characters for
recent attempt at a phylogenetic reconstruction, Milner extinct families (Fig. 17-1). The assumptions are based
(1983) used only selected characters and misinterpreted on association. For example, in all cladograms using only
the polarities of some of those characters. characters known for the extinct families, all extinct fam-
Five data sets were used to genérate cladograms: ilies except the Karauridae are placed within living fam-
ilies that have internal fertilization; therefore, infernal fer-
1. Recent families using 37 characters (all char- tílization is assumed for all extinct families except the
acters except autapomorphies restricted to Karauridae.
extinct families—FF, HH-JJ); consistency ín- This phylogenetic arrangement has a slightly higher
dex = 62.6%. consistency Índex than any other cladogram generated.
2. All families using 23 characters (only those for Moreover, the Sírenidae has only three reversáis and one
which data are available for extinct families); convergence, the lowest of any arrangement. However,
consistency Índex = 65.9%. there ¡s an unresolved trichotomy involving the Proteidae
3. Recent families using only those 23 characters and the stem leading to the Batrachosauroididae and
available for all families; consistency Ín- Prosirenidae. Before a better phylogeny of salamanders
dex = 70.5% can be generated, it is necessary to reevaluate certain
4. Recent families using 27 characters (those that characters (especially with respect to paedomorphosis)
are not strongly paedomorphic—A-C, E-H, and to add new characters that pertain to all families.
EVOLUTION
466

Figure 17-1. Hypothesized

phylogenetic relationships among the
families of salamanders based on
nonpaedomorphic characters.
Phylogeny of Recent families
reconstructed by WAGNER78
program using 27 characters;
consistency Índex = 73%.
Approximate arrangement of extinct
families (dashed lines) based on
known character states and assumed
States for characters E, F, K, P, BB,
CC, LL, MM, and NN. See Table
17-1 for character states and text for
descriptions of characters and
polarities. Tick marks indícate places
of shifts in characters to states
indicated by subscripts; X's indícate
reversáis.

GYMNOPHIONA ondary orthoplicate annuli throughout the length of the

body is considered to be primitive (0). Sequenüally de-
Character States rived states are primary and secondary annuli present
The characters and their transformatíon series (Table 17- throughout the length of the body but anterior annuli are
2) are based primarily on Nussbaum (1977, 1979a). not orthoplicate (1), secondary annuli are absent ante-
A. Tai/.—A tail is present primiüvely in tetrapods and riorly or throughout the length of the body (2).
salamanders. The presence of a tail in caecilians is con- E. Sea/es.—Scales are present in the annular folds of
sidered to be primitive (0); the absence of a tail is derived many caecilians (E. Taylor, 1972). Using the argument
(1). of cephalization, Nussbaum (1977) considered the pres-
B. Mouth Opening.—Some caecilians have a termi- ence of scales in annular folds throughout the length of
nal mouth like that of labyrinthodonts, whereas others the body to be primitive (0). Reduction in size and num-
have a projectíng snout with a recessed mouth, a con- ber or complete absence of scales is derived (1).
dition reflecting a specialization for burrowing. A terminal F. Premaxilla-Nasal.—These bones are primitively
mouth is considered to be primitive (0). Serially derived paired, sepárate elements in amphibians. This is regarded
states are subterminal (1) and recessed (2). as the primitive state in caecilians (0). The fusión of the
C. Eye-Tentacle Relationship.—The tentacle devel- nasals and premaxillae into paired nasopremaxillae is a
ops in the nasolacrimal duct and migrates varying dis- derived state (1) that results in a more rigid rip of the
tances anteriorly away from the eye during ontogeny. A snout as a specialization for burrowing.
tentacular opening adjacent to the anterior edge of the G. Septomaxilla.—Primitively, these small bones are
eye is considered to be primitive (0). A more anterior distinct, sepárate elements in lissamphibians. Within the
position ¡s derived (1). A secondarily derived condition caecilians, the presence of sepárate septomaxillae is
is the anterior translocaüon of the eye on the tentacle primitive (0); their loss or fusión to adjacent bones is
(2). derived (1).
D. Annulation.—Caecilians have annular grooves. In H. Prefrontal.—These paired bones characteristically
some groups there are primary and secondary annuli are present primitively in tetrapods. This is the primitive
throughout the length of the body, whereas in others state (0) in caecilians. The loss or fusión of the prefronta!
secondary annuli are present only posteriorly or are ab- with the maxillopalatine is a derived state (1).
sent. Also, in some caecilians having primary and sec- I. Squamosal-Frontal Articulation.—Primitively in
ondary annuli, the annuli are orthoplicate (in the same tetrapods, as well as nearly all vertebrates, the squamosal
plañe around the body) throughout the length of the does not articúlate with the frontal; this is the primitive
body; others are orthoplicate only posteriorly or not or- state in caecilians (0). The articulation of the squamosal
thoplicate anywhere on the body. Nussbaum (1977) based and frontal is a derived state (1) that increases skull rigidity
the polarity of this character on the argument of cephal- as an adaptation for burrowing.
izaüon. Accordingly, the presence of primary and sec- J. Temporal Fossa.—Nussbaum (1977) argued that
 Phylogeny
stegokrotaphy (complete skull roofing) is secondarily de- This is considered to be the primitive state (0); an un- 467
rived in caecilians; this conclusión was supported by the perforated columella is derived (1).
developmental studies of M. Wake and Hanken (1982). O. Quadrate-Maxillopalatine Articulation.—The
Thus, in caecilians, the presence of a temporal fossa be- quadrate articúlales with the maxillary via the jugal and
tween the parietal and squamosal (zygokrotaphy) is prim- quadratojugal (or simply the latter) primitively in tetra-
itive (0), whereas the juxtaposition of these elements is pods. In some caecilians, the articulation is directly be-
derived (1). rween the quadrate and the maxillopalatíne via an an-
K. Vomer.—The vomers are separated by the cultri- terior process of the quadrate, which may represen! the
form process of the parasphenoid portíon of the básale quadratojugal. This is considered to be the primitíve state
in some caecilians. This is considered to be the primitíve (0). The absence of a bridge between, or articulation of,
state (0). In other caecilians, the vomers are in contact the quadrate and maxillopalatine is derived (1).
for nearly their entire lengths; this lends rigidity to the P. Retroarticular Process.—The retroartícular process
skull and is considered to be the derived state (1). of the pseudoangular is short and horizontal in some
L. Parasphenoid Architecture.—The sides of the caecilians. This is the primitive state (0). A long process
parasphenoid portion of the básale in salamanders, anu- curving upward is a specialization for jaw closing and is
rans, and some caecilians are parallel. This is considered derived (1).
to be the primitíve state (0). The anterior convergence of Q. Larvae.—The presence of a larval stage is primi-
the sides of the parasphenoid región is derived (1). tíve for vertebrales. Thus, presence of larvae is primitive
M. Pterygoid.—These bracing bones are present (0), whereas direct development is derived (1).
primitívely in tetrapods. Their presence as disttnct ele- R. Body Shape.—Most caecilians have round bodies
ments is primitive (0) in caecilians. Fusión of the ptery- in cross section; this is considered to be the primitíve state
goid with the maxillopalatíne or quadrate is derived (1), (0). Lateral compression of the body posteriorly in ty-
and absence of pterygoids is secondarily derived (2). phlonectids is an obvious aquatic specialization and is
N. ColumeUar Perforation.—Primitively in tetrapods, derived (1).
the columella (stapes) is pierced by the stapedial artery. S. Eye.—The usual position of the eye in vertebrales

Table 17-2. Distribution of Character States in Families of Caec¡l¡ansab

j
1
i •v19
thyophüdae

1
S t ;
1
a
e 1 :
Character i £ 1 1 j* 3
A. Tail 0 0 0 1 1 1
B. Mouth opening 0 1 2 2 2 2
C. Eye-tentacle relationship 0 1 1 2 1 1
D. Annulaüon 0 1 1 2 2 2
E. Scales 0 0 1 1 1 1
F. Premaxilla-nasal 0 0 0 0 1 1
G. Septomaxilla 0 0 0 0 1 1
H. Prefrontal 1 0 0 0 1 1
I. Squamosal-frontal articulation 0 1 1 0 1 1
J. Temporal fossa 0 1 1 1 1 1
K. Vomer 0 1 1 1 1 1
L. Paraspenoid architecture 0 1 1 1 1 1
M. Pterygoid 0 0 0 2 1 1
N. ColumeUar perforation 0 0 0 0 1 1
0. Quadrate-maxillopalatine articulation 0 1 1 1 1 1
P. Retroarticular process 0 0 0 1 1 1
Q. Larvae 0 0 0 1 1 1
R. Body shape 0 0 0 0 1 0
S. Eye 0 0 0 1 0 0/1
T. Dorsolateral processes of básale 1 0 0 0 0 0
U. Columella 0 0 0 1 0 0
V. Anal claspers 0 0 0 0 1 0
°0 = primitive; 1,2 = derived.
bSee text for definiüons of states.
EVOLUTION
468 ¡s ¡na bony socket. This is the primitive condition (0), as cause two or more characters seem to represent highly
contrasted with the derived state (1) of having the eye correlated changes in a single funcüonal complex. There-
covered by bone as ¡n scolecomorphids and some cae- fore, in the latter cases, the complex is treated as a single
ciliids. character.
T. Dorsolateral Processes of Básale.—These The hypothesized phylogenetic relatíonships agree with
processes are absent in primitive tetrapods and most cae- Nussbaum's (1977) scenario that ancestral caecilians re-
cilians (0). Their presence (1) in an otherwise weak skull sembled rhinatrematids by having highly kineüc, zygo-
is a uniquely derived state in rhinatrematíds. krotaphic skulls with a full complement of bony elements.
U. Columella.—A columella is present primiüvely in The primitive caecilians had aquatic larvae. This mode
tetrapods (0). The absence of this bone in scolecomor- of life history was maintained in ichthyophiids and uraeo-
phids is derived (1). typhlids, which are more active burrowers with stego-
V. Anal Claspers.—This type of modified anal región krotaphic skulls. Highly specialized burrowers with min-
is unknown in tetrapods except in some typhlonectid cae- imally kinetíc skulls and terrestrial eggs undergoing direct
cilians. An unmodified vent is primitive (0), and the pres- development or viviparity evolved from uraeotyphlid-like
ence of anal "claspers" is derived (1). ancestors. The aquatic typhlonectids have the burrowing
specializations of caeciliids and presumably evolved from
Phylogeny a caeciliid-like ancestor, a hypothesis not rejected by any
Nussbaum (1977, 1979a) demonstrated that the Rhina- autapomorphies of the Caeciliidae.
trematidae is characterized by a suite of primitive char-
acter states and one autapomorphy. The ichthyophiids
and uraeotyphlids possess a combination of primitive and ANURA
derived character states; neither family has autapomor- For purposes of discussion, generally accepted suprafa-
phies, so the historical reality of these groups is not as- milial categories are used, but with the clear understand-
sured. The other three families of caecilians form a group ing that such categories are not necessarily monophyletic;
characterized by many derived character states. Three these categories are simply groupings of families. These
autapomorphies are present for the scolecomorphids and descriptors are: (1) discoglossoid including the Leiopel-
two for the typhlonectids. No autapomorphies charac- matidae and Discoglossidae; (2) pipoid including the
terize the Caeciliidae; although it is probably not a his- Rhinophrynidae, Pipidae, and Palaeobatrachidae; (3)
torical group, it is retained here. A phylogenetíc recon- pelobatoid including the Pelobatidae and Pelodytidae;
structíon using 21 characters has a consistency Índex of (4) microhylid containing only the Microhylidae; (5) ran-
89.6% (Fig. 17-2). In this reconstruction, many charac- oid including the Ranidae, Rhacophoridae, and Hyper-
ters used by Nussbaum (1977, 1979a) were omitted either oliidae; and (6) bufonoid containing all of the other fam-
because their states are unknown in many genera or be- ilies.

Figure 17-2. Hypothesized

phylogenetic relationships of the
families of caecilians based on 21
characters and reconstructed by the
WAGNER78 program. See Table
17-2 for character states and text for
descriptions of characters and
polarities. Tick marks indícate places
of shifts of characters to states
indicated by subscripts; X's indicate
reversáis. One convergence
(character H) exists in the
Rhinatrematidae and the lineage
leading to the Caeciliidae and
Typhlonectidae, and another
convergence (character S) exists in
the Scolecomorphidae and
Caeciliidae (some genera only). One
reversal (character I) exists in the
Scolecomorphidae. Consistency
Índex = 89.6%.
 Phylogeny
Character States cartilages are partially free, resulting in a so-called pseu- 469
A. Vertebral Co/umn.—Noble (1922, 1931b) based doarciferal girdle. On the bases of ontogenetic and dis-
his classificaüon of anurans chiefly on the nature of the tributional evidence, it seems clear that both pseudofir-
intervertebral joints, characters that were derived from misterny and pseudoarcifery are derived, homoplasious
the work of Nicholls (1916). The distribution of amphi- features; thus, only firmisterny and arcifery are used in
coelous, anomocoelous, procoelous, and opisthocoelous the phylogenetic reconstruction presented here. An ar-
vertebral joints (Table 17-3) suggests that these vertebral ciferal girdle is considered to be primitive (0), whereas a
states are homoplasious. Mookerjee (1931) and Griffiths firmisternal girdle is derived (1).
(1963) described patterns of vertebral development that D. Other Features of the Pectoral Girdle.—In ad-
resulted in different kinds of vertebral centra. Perichordal dition to the primary architecture, other features of the
central are round in cross section, whereas epichordal pectoral girdle that have been employed in anuran phy-
centra are depressed in cross section. Griffiths described logenetic reconstructions include characters of the pre-
hollow perichordal centra as ectochordal and solid peri- and postzonal pectoral elements—presence or absence
chordal centra as holochordal. He designated epichordal and degree of ossification of the omosternum and ster-
centra as stegochordal and described two developmental num (mesosternum and xiphisternum) (see J. D. Lynch,
pathways that resulted in indistinguishable stegochordal 1973, for discussion). The presence of a sternum in prim-
vertebrae in adult anurans. In their critique of Griffiths itive tetrapods, salamanders, and rriost anurans suggests
(1963), Kluge and Farris (1969) pointed out that the that its absence in Rhinophrynus and Brachycepha/us is
degree of epichordy as defined by Mookerjee (1931) and a derived feature. An omosternum is present or absent
Mookerjee and Das (1939) is variable among the rela- in arciferal anurans, and tends to be elaborated in fir-
tively few taxa of anurans that have been examined. misternal anurans that do not have reduced girdles (i.e.,
Moreover, Griffiths (1963) defined two types of stego- some microhylids). Because primitive arciferal anurans
chordy (= epichordy) based on different developmental possess an omosternum, its presence is assumed to be
patterns. Owing to the incomplete knowledge of the de- primitive among anurans. Its loss among other arciferal
velopmental patterns and their distribution and variaüon anurans and some firmisternal frogs, as well as its elab-
among anurans, it is impossible to establish the polarities oration among firmisternal frogs are presumed to be de-
of the transformation series of the various vertebral types rived states.
at this time. The foregoing characters are discussed in Most of the anurans have a clavicle that articulates with
more detail in Chapter 13. the scapula anterior to the glenoid fossa. According to
Many other vertebral characters have been used in Kluge and Farris (1969), the distal end of the clavicle
phylogenetic reconstruction by various investigators overlays the scapula anteriorly in primitive tetrapods. In
(e.g., J. D. Lynch, 1973), but the distributions of many anurans, this condition is considered to be primitive (0);
of these within family groups is inconsistent, and within nonoverlap of the scapula by the clavicle is derived (1).
nominal families there is variation in many of them (Table E. Cranium.—There is considerable variation in the
17-3). cranial elements of anurans, including reduction or loss
The only vertebral character included in the phyloge- of the vomers, palatines, quadratojugals, and columellae
netic reconstruction offered herein is the reduction in the in diverse groups. The premaxillae and maxillae are den-
number of presacral vertebrae. In anurans, a greater tate in most anurans, but edentate in rhinophrynids, bu-
number of presacral vertebrae is considered to be prinn- fonids, brachycephalids, rhinodermatids, and most mi-
itive because Triadobatmchus has 14 presacrals, and sal- crohylids; some taxa in other families also are edentate.
amanders and caecilians have even more. Nine presacral The absence of teeth is considered to be a derived fea-
vertebrae is considered to be primitive (0), and eight or ture. Because palatines are present in salamanders and
fewer to be derived (1). all extinct orders of amphibians, their absence in anurans
B. Ribs.—Ribs are characteristic of vertebrates. The is considered to be derived (1) and their presence prim-
presence of free dorsal ribs in adult anurans is considered itive (0).
to be primitive (0), and their absence derived (1). F. Parahyoid.—A parahyoid bone associated with the
C. Basic Pectoral Gírale Architecture.—Develop- cartilaginous hyoid píate is present in discoglossoids, pa-
mentally and structurally, anurans have either an arciferal laeobatrachids, Rhinophrynus, and Pe/odytes. Although
or firmisternal pectoral girdle as explained in Chapter 13. there is no record of its occurrence among other am-
Griffiths (1963) argued, probably correctly, that arcifery phibians, De Beer (1937) suggested that the parahyoid
(characteristic of salamanders and most anurans) is prim- in Polypterus and teleostean fishes is homologous with
itive, and that firmisterny is a derived feature character- the same element in anurans. The nature of this ossifi-
istic of ranoids, microhylids, and dendrobatids. In some cation is highly variable and has not been investigated in
developmentally arciferal anurans, the epicoracoid car- detail. In some frogs it seems to be an irregularly shaped
tilages fuse medially to produce a pseudofirmisternal gir- ossification associated with the cartilage of the hyoid píate
dle; conversely, in a few firmisternal taxa, the epicoracoid and may be single and median (e.g., Leiopelma hoch-
Table 17-3. Vertebral Characteristics oí Anuran Families0

Number of Presacrals Neural Atlanta! Sacro- Transverse

presacral I and U Vertebral Centrum arches cotyles Free Sacral coccygeal processes
Family vertebrae fused type6 typec imbrícate juxtaposed ribs diapophyses articulation on coccyx

Brachycephalidae 7 + • P H/? • + - Dilated Bicondylar -

Bufonidae 5-8 ± P H/Pc + + - Dilated Bicondylar -
Centrolenidae 8 P H/? Dilated Bicondylar -
Dendrobatidae 8 P H/? - - Cylindrical Bicondylar +
Discoglossidae 8 - 0 S/Pc, Ep + + +d Expanded Bicondylar +
Heleophrynidae 8 A E/? + + — Cylindrical Bicondylar -+•
Hylidae 8 - P H/Pc, Ep ± Dilated" Bicondylar -
Hyperoliidae 8 P/D H/? ± . - - Cylindrical Bicondylar -
Leiopelmatídae ^ 9 - Am , E/Pe + + .' Dilated Conüguous +
Leptodactylidae ; 8 - P H/Pc, Ep ± ± - Cylindrical Bicondylar ±
Microhylidae " : 8 ;:: - P/D H/Pc ± - :: Dilated Bicondylar' —
Myobatrachidae 8 ± A/P H/? ± ± - Dilated Bicondylar ±
tPalaeobatrachidac 7-8 - + P S/? + + +9 Dilated Bicondylar ±
Pelobatidae '- 8 ' A S/? + + - Expanded Monocondylar' + f
Pelodytidae 8 + - A S/? + + - Expanded Monocondylar +
Pipidae 6-8 ± 0 S/Ep + ± +3 Expanded Fused -
Pseudidae 8 P H/Pc + - Cylindrical Bicondylar -
Ranidae 8 ± P/D H/Pc ± - - Cylindrical Bicondylar -
Rhacophoridae 8 P/D H/Pc, Ep - - Cylindrical Bicondylar -
Rhinodermatidae 8 + P H/? + + - " Dilated Bicondylar —
Rhinophrynidae 8 0 E/Pe + + - Expanded Bicondylar -
Sooglossidae 8 P H/? + - Dilated Monocondylar +
°Symbols are as follows: bSensu Noble (1922).
+ = Presence of a structure in a family. cSensu Griffiths (19631/sensu Kluge and Farris (1969).
- = Absence of a structure in a family. dAnkylosed to transverse processes in Bombira.
± = Variable in a family. eCylindrical in some.
A = Amphicoelous or procoelous with free intervertebral bodies at some stage of development. ffused in some.
Am = Amphicoelous with contiguous intervertebral cartilage. 9Ankylosed to transverse processes in adults.
D = Diplasiocoelous.
E = Ectochordal.
Ep = Epichordal.
H = Holochordal.
P = Procoelous.
Pe = Perichordal.
S = Stegochordal.
 Phylogeny
stetteri or paired and lateral (e.g., Bombina variegata). In number of digits is characteristic of the Brachycephalidae. 471
Rhinophrynus, in contras!, the parahyoid is a transverse, Such decreases in the phalangeal elements are inter-
shallowly V-shaped bone that extends across the width preted as derived, paedomorphic events. An increase in
of the ventral surface of the hyoid píate. The functíon of the phalangeal formula by the addition of intercalary ele-
the parahyoid bones is unknown, as are details of their ments (usually short and cartilaginous) between the pen-
development. Thus, at this time, it is not possible to make ultimate and terminal phalanges characterizes pseudids,
an unequivocal statement about their homologies. Based hylids, centrolenids, rhacophorids, hyperoliids, phrynom-
on the occurrence of a parahyoid in some fishes, the erine microhylids and mantelline ranids. Absence of in-
presence of this element in anurans is considered to be tercalary elements is considered to be a primitive state
primitive (0) and its absence derived (1) shared by salamanders and anurans (0), whereas their
G. Cricoid Cartilage.—In most anurans, the carti- presence is derived (1).
laginous cricoid ring of the larynx is complete in adults, K-L. Thigh Musculature.—As a result of Noble's
and arises from paired cartílaginous structures. In myo- (1922) study, characteristics of thigh musculature have
batrachines and sooglossids, the ventral portions of the been used widely in phylogenetic analyses of anurans. J.
paired cartilages fail to unite, whereas in Rhinophrynus D. Lynch (1973) used only five features of the thigh
and pelobatoids, the dorsal portions of the paired carti- musculature in his analysis: (1) the presence of the m.
lages do not unite. Assuming that the paired cartilaginous caudalipuboischitibialis, (2) the presence of an accessory
elements in early developmental stages of anurans are tendón of the m. glutaeus magnus, (3) the presence of
homologous with the lateral cartilages that support the an accessory head of the m. adductor magnus, (4) the
laryngotracheal chamber in salamanders, paired carti- position of the insertion of the m. sartoriosemitendinosus
lages as occur in early development are considered to be relative to the m. gracilis, and (5) the condition of the m.
primitive in amphibians (0). A complete cricoid ring is semitendinosus-m. sartorius complex. Dunlap (1960) in
derived (1). The failure of the cricoid cartilages to unite his comparative study of the thigh musculature of several
dorsally or ventrally is assumed to be a paedomorphic species of anurans documented the significant variation
event that results in two independently derived states— in the occurrence and sizes of accessory heads and ex-
ventral gap in the ring (O') and dorsal gap in the ring tents of muscle insertions among anurans. This variation
(O"). coupled with the fact that such information is available
H. Tongue.—Tongues are present in all amphibians for relatively few species suggests that most of these char-
except the pipid frogs, which retain vestiges of the lingual acters are not amenable to phylogenetic interpretation at
musculature. The presence of a tongue is primitive (0), present. Although the occurrence of these characters in-
and its absence is derived (1). sofar as they are known is listed in Table 17-4, only two
I. Astragalus and Calcaneum.—In salamanders and are used in this analysis.
Triadobatrachus, the fibulare and tibíale (the astragalus K. Caudalipuboischiotibialis muscle.—Noble (1922)
and calcaneum, respectively, of Recent anurans) are sep- concluded that the m. caudalipuboischiotibialis was ho-
árate tarsal elements. In anurans, tríese elements are mologous with the muscle of the same ñame in sala-
elongated and fused proximally and distally in most taxa; manders and that its presence only in leiopelmatids among
the astragalus and calcaneum are fused throughout their all living anurans is primitive (0), and its absence is de-
lengths in only two families—the pelodytids and centro- rived (1).
lenids. Incomplete fusión of the astragalus and calca- L. Semitendinosus-sartoríus muscle complex.—The
neum is assumed to be primitive (0), whereas complete m. semitendinosus in anurans is homologous with the m.
fusión of these bones is derived (1). puboischiotibialis, an undivided thigh muscle in salaman-
J. Hands and Feet.—J. D. Lynch (1973) considered ders. In most anurans, a sepárate muscle, the m. sarto-
the number of tarsalia to be an important feature, with rius, is differentiated from the m. semitendinosus. Kluge
the presence of three tarsalia being primitive and the and Farris (1969) suggested that the differentiation of the
presence of two being derived. Salamanders have up to m. sartorius from the m. semitendinosus represents a
four free tarsalia, suggesting that the greater number of continuum and rejected the use of the character in phy-
free elements in anurans is primitive. Fusión of Tarsalia logenetic analysis. The two muscles are only partially sep-
2, 3, and 4 has occurred to produce two tarsals (i.e., arated in Discog/ossus, Xenopus, and Limnodynastes.
1 + 2-4) in most anurans. In Triadobatrachus, discog- Otherwise, in those anurans that have been examined
lossoids, pelodytids, rhinodermatids, mantelline ranids, only one muscle, the m. semitendinosus, is present or
and hyperoliids, and some arthroleptine and astyloster- both muscles are discrete. Because of the single condition
nine ranids, there are three tarsalia (i.e., 1 + 2 + 3—4) in salamanders, the absence of a discrete m. sartorius in
owing to the lack of fusión of Tarsal 2 with Tarsalia 3 anurans is considered to be primitive (0), whereas the
and 4. presence of a discrete m. sartorius is derived (1).
The normal phalangeal formulae in anurans is 2-2-3- M. Trigémina/ and Facial Ganglio.—As explained
3 (hand) and 2-2-3-4-3 (foot). Reduction in the number by Sokol (1975) in his paper on the phylogeny of anuran
of phalanges occurs in a few taxa, and a reduction in the larvae, two states pertain to the ganglia of the trigeminal
EVOLUTION
472 and facial nerves (C.Nn. V and VII, respectively). In sal- morphological features of these types are discussed in
amanders and all anurans with Type III larvae, the tri- more detail in Chapter 6. Type I is characteristic of the
geminal and facial ganglia are sepárate, and the major pipoidea, Type II the microhylids, Type III the discoglos-
rami of the facial nerve exit the chondrocranium via the soids, and Type IV all other anurans. Sokol (1975) sug-
palatine foramen, which lies lateral and slightly posterior gested that Types III and IV were derived independently
to the prootic foramen; the cartilage separatíng the two from a common ancestor. The opercular structure is de-
foramina is termed the prefacial commissure. In all other rived in Types I and II; the m. interhyoideus posterior
anurans surveyed, the ganglia of the trigeminal and facial muscle is absent, and the ceratobranchial is fused with
nerves are fused to form the single prootic ganglion. the hyobranchial píate. Because Types I, II, and IV share
The rami of both nerves emerge via the single prootic the derived feature of a single prootic ganglion (see dis-
foramen which is located immediately anterior to the cussion above), it is assumed that Types I and II are
otic capsule. Anurans having sepárate trigeminal and independent derivatives of larval Type IV. Larval Types
facial ganglia are primitive (0), whereas those in which I and II share many specialized morphological features in
the ganglia are fused to form a prootic ganglion are de- the structure of the chondrocranium, the filter apparatus,
rived (1). and the hyobranchial skeleton; moreover, neither type
N. Bidder's Organ.—In all male bufonid larvae the bears keraünized mouthparts.
anterior portíon of each gonad becomes enlarged to form However, Type I and Type II larvae are distinguished
a Bidder's organ, which consists of ovarían tíssue. In some by the structures of the opercula, the modes of fusión of
genera (namely Bu/o, Pedostibes, Pseudobufo, Atelopus, the hyobranchial apparatus, and the architecture of the
Leptophryne, Dendrophryniscus, Nectophryne, some suspensoria. Type I larvae also differ from Type II larvae
species of Nectophrynoides), Bidder's organ is retained in the absence of interna! gills and the third interbranchial
in the adult males in association with the testis as either septum in the former. The coding of larval types follows
a peripheral, lateral band of ovarían tíssue or a cap over the suggestion of Sokol (1975) wherein a hypothetical
the anterior pole of the testis (M. Wake, 1980a). Reten- ancestral type is considered to be primitive (0). Types III
tíon of Bidder's organ in adult bufonids seems to be a and IV are independently derived and are coded as (1)
paedomorphic event (Griffiths, 1959b). Absence of this and (I 7 ), respectively. Types I and II are independently
structure in anurans is considered to be primitive (0), and derived from Type IV and are coded as (2) and (2').
its presence in bufonids derived (1). P. Amplectic Position.-^í. D. Lynch (1973) argued
O. Larval Types.—As proposed by Orton (1957), convincingly that inguinal amplexus, as it occurs in all
modified by P. Starrett (1973), and elaborated by Sokol discoglossoids, pipoids, pelobatoids, heleophrynids,
(1975), there are four types of anuran larvae. The sooglossids, and myobatrachine myobatrachids (also in

Table 17-4. Characteristics of the Thigh Musculature in Anuran Families

M. caudali- M. semitendinosus Insertion Accessory Accessory

puboischiotibialis sepárate from of tendón of tendón of head of
Family present m. sartorius m. semitendinosus" m. glutaeus magnus m. adductor magnas

Brachycephalidae + V + +
Bufonidae + V + +
Centrolenidae + V - +
Dendrobatidae + P + +
Discoglossidae ± V ±
Heleophrynidae + V + +
Hylidae + V +
Hyperoliidae + D +
Leiopelmatídae + V -
Leptodactylidae + P, V + +
Microhylidae + D +
Myobatrachidae + D, P, V + +
Pelobatídae V + —
Pelodytídae V +
Pipidae ± P +
Pseudidae + V + +
Ranidae + D ± +
Rhacophoridae + D +
Rhinodermatidae + V +
Rhinophrynidae + P - -
Sooglossidae - + D +
*D = dorsal, P = penetraüng, V = ventral to m. gracilis.
 Phylogeny
473

Figure 17-3. Hypothesized

phylogenetic relationships of the
families of anurans based on 16
characters and reconstructed by the
WAGNER78 program. See Table
17-5 for character states and text for
descriptions of characters and
polarities. For purposes of analysis,
the states of characters, G, L, M, and
O of the extinct family
Palaeobatrachidae were coded the
same as those of Pipidae; also
character N in the Brachycephalidae
and Sooglossidae was coded the
same as other bufonoids. Tick marks
indícate places of shifts of characters
to states indicated by subscripts. Two
convergences exist in each of seven
characters (A, B, G, I, J, K, and L),
and three convergences occur in
character F. Consistency índex =
65.6%.

two genera of telmatobiine leptodactylids) is primitive (0). Developmental Pattern. Reproductivo modes are
Sequentially derived states are axillary (1) and cephalic highly diverse in anruans. The presumed primitive mode
(2). In addition to these types of amplexus, there are is the deposition of eggs and development of larvae in
deviations based on body morphs and behavior (see ponds; 28 advanced modes are recognized (see Chapter
Chapter 3). 2). Although some families are characterized by derived
modes (e.g., transportation of larvae in vocal sac in rhi-
nodermatids, transportation of tadpoles on dorsum in
Other Characters dendrobatids, or arboreal eggs and stream tadpoles in
Numerous other characters have been used in phyloge- centrolenids), other families have diverse modes (Table
netic reconstructions of anurans. However, they have not 2-3). It is evident that some of the derived reproductive
been used here because either (1) the direction of evo- modes, such as direct development of terrestrial eggs,
lutionary change has not been determined, (2) the dis- have evolved independently in different lineages of anu-
tribution of the character states among anurans is insuf-
rans. Thus, developmental pattern is useful phylogenet-
ficiently known, or (3) the character states apparently ically within lineages, but not for discerning relationships
have arisen so many times that the character cannot be among anurans as a whole.
used to show relationships. In addition to numerous char-
acters that were rejected above, the following merit dis- Chromosome Complement. Although karyotypes
cussion. are known for a great variety of anurans representing all
families (Table 16-3), few generalities can be made re-
Pupil Shape. As noted by J. D. Lynch (1973), anu- garding chromosomal evolution in anurans. Microchro-
rans have four shapes of the pupil: (1) triangular (only mosomes occur only in discoglossoids. With the excep-
in discoglossids), (2) round (only in pipids and some mi- tion of Xenopus, the basic karyotype of other groups of
crohylids), (3) horizontal (most bufonoids, microhylids, anurans seems to be 2N = 26 bi-armed chromosomes.
and ranoids), and (4) vertically elliptical (some disco- This number is reduced, presumably by centric fusión, in
glossoids and pipoids, pelobatoids, heleophrynids, most many lineages and increased by centric fission in a few
hyperoliids, and some myobatrachids, leptodactylids, hy- groups (see Chapter 16).
lids, microhylids, and ranids). Although J. D. Lynch (1973)
conceded that pupil shape might be adaptive, he con- Phylogeny
cluded that the vertical pupil is primitive and the other As emphasized in the foregoing discussion of characters,
shapes are independently derived. existing knowledge of the taxonomic distribution and the
 17-5. Distiibution of Character States in Families of Anurans"

1
|

j a 4
}
„
a
j 4?. 9 1 g
tt

Jí
0
V

Character .. £ &
•§
u 0 5 X X 1 3 2 i ^t a. s. £ £ £ 1 a a s <ñ
A. Vertebral column '•• i 1 1 1 i 1 1 1 0 i 1 1 1 1 i 1 1 1 1 i 1 1
B. Ribs i 1 1 1 0 1 1 1 0 i 1 1 0 1 i 0 1 1 1 i 1 1
C. Basic pectoral girdle 0 0 0 ': 1 0 0 0 1 0 0 1 0 0 0 0 0 0 1 1 0 0 0
architecture
D. Other features of the -• i 1 i •••' 1 0 1 1 1 0 i 1 1 0 i i 0 1 1 1 i 0 1
pectoral girdle
E. Cranium 0 0 0 ', 0 1 0 0 0 1 0 0 0 1 0 0 1 0 0 0 0 1 0
F. Parahyoid 1 1 i 1 0 1 1 1 0 i 1 1 0 1 0 1 1 1 1 i 0 1
G. Cricoid cartílage 1 1 i 1 1 1 1 1 1 i 1 0' ? 0" 0" 1 1 1 1 i 0" 0'
H. Tongue 0 0 0 0 0 0 0 0 0 0 0 0 ? 0 0 1 0 0 0 0 0 0
I. Astagalus and calcaneum 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0
J. Hands and feet 0 0 1 0 0 0 1 1 0 0 oc 0 0 0 0 0 1 od 1 0 0 0
K. Caudalipuboischio- 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 1 1 1 1 1
tíbialis muscle
L. Semitendinosus-sartorius 1 1 1 1 0 1 1 1 0 1 1 1 ? 0 0 0 1 1 1 1 1 1
muscle complex
M. Trigémina! and facial 1 1 1 1 0 1 1 1 0 1 1 1 ? 1 1 1 1 1 1 1 1 1
ganglia
N. Bidder's organ 0 1 0 0 0 0 0 0 0 0 0 0 ? 0 0 0 0 0 0 0 0 0
O. Larval types — r 1' r 1 r 1' 1' 1 1' 2' 1' 2
iopelmatidae r r 2 1' V r r 2 —
P. Amplectic positíon 1 i 1 2 0 0 1 1 0 1" 1 0' ? 0 0 0 1 1 i i 0 0
°0 = primitive; 1, 2, etc.; ? — unknown; — not applicable.
'See text for definitions of states.
cDerived state ¡n phrynomerines.
dDerived state in mantillines.
ePrimitive state in some telmatobiines.
CDerived state (1) in limnodynastines.
robatrachidae

alaeobatrachidae

lobatidae

lodytidae
 Phylogeny
475

Figure 17-4. Hypothesized

phylogenetic relationships among
firmisternal anurans. Characters C,
J, and P are the same as in Table
17-5 and Figure 17-3. Character Q is
the number of tarsalia; according to
J. D. Lynch (1973), the primitive
state is three tarsalia (0), and the
derived state (1) occurs in niost
firmisternal anurans. The tadpole of
scaphiophrynines is intermedíate
between Type II of microhylids and
Type IV of other firmisternal anurans
(Wassersug, 1984).

direction of evolutionary change in many characters limits It is evident that intercalary elements in the digits
the number of characters that can be used in phyloge- (Character J) evolved at least twice—once in an arciferal
netic reconstruction. Consequently, only 16 characters lineage and again in firmisternal frogs. The cladogram is
were coded for phylogenetic analysis (Table 17-5). A over-simplified with respect to this character, for inter-
cladogram generated from these character states (Figure calary elements are present in mantelline ranids and
17-3) has eight homoplasious characters and a consist- phrynomerine microhylids. Also, not all microhylids have
ency Índex of 65.6%. typical Type II tadpoles (see Chapter 6). Thus, if subfa-
Several unresolved polytomies exist in this cladogram. milial groups are analyzed with respect to these charac-
If the exceptíons in amplectic position (Character P) noted ters, and some other characters, a somewhat different
in Table 17-5 were shown on the cladogram, both groups cladogram is generated (Fig. 17-4).
of bufonoids would be rearranged. The limnodynastine The distribution of some character states and the po-
myobatrachids would cluster with the leptodactylids, and sition of some families in the cladogram pose some other
two genera of leptodactylids, Batmchyla and Pleurodema questions. A single synapomorphy unites the Rhino-
(in part) would be associated with the myobatrachids. phrynidae with the Pipidae and Palaeobatrachidae, but
Thus, the bufonoids are a group of families that are dis- this results in three convergences in the rhinophrynids
tinguished from the ranoids and microhylids by the struc- and other lineages. Furthermore, one of these homopla-
ture of the pectoral girdle. The elucidation of relationships sious character states (Character G) is the only synapo-
among the bufonoid families is a prerequisite to a realistic morphy unitíng the Pelobatidae and the Pelodytidae. Ad-
phylogenetic reconstruction of anurans; certainly, no sys- ditional characters are needed to resolve the relationships
tematic problem dealing with amphibians is more de- of the rhinophrynids with the pelobatids and pelodytids.
serving of intensive research. There are some distinctive differences between the pe-
An obvious difference between this cladogram and most lobatine and megophryine pelobatids (see account of Pe-
phylogenetic arrangements is the placement of the den- lobatidae in Chapter 19). Resoluüon of the phylogenetic
drobatids with the ranids, as originally suggested by Grif- relationships of taxa included in the Pelobatidae may shed
fiths (1959a). This association is based on the synapo- light not only on the relationships of the so-called prim-
morphy of the firmisternal pectoral girdle (Character C). itive anurans but also between these and the myoba-
Dendrobatids are like ranids in all characters coded ex- trachids. The Myobatrachidae contains two distinctive
cept amplectic position; dendrobaüds have a secondarily subfamilies, the Myobatrachinae and the Limnodynas-
derived state of amplectic position. Dendrobatids also share tinae. Possibly these are not sister groups.
with ranids round sacral diapophyses, but they are dis- Although not all branches on the cladogram are marked
tinguished by the habit of carrying tadpoles on the dor- with apomorphies, characters do exist to define each of
sum. the families (see Chapter 19).
 CHAPTER 18
The most striking feature ofpast and
present distributions [of amphibians] is the
"iindamental and consistent association of
distributions ofeach group with eilher
Laurasia or Gondwanaland, and those "
supercontinent's Cretaceous fragmente that
bv continental drift have conté to form
today's major land áreas.
Biogeography
JayM. Savage (1973)

. ewV scienüfic discoveries have influenced historical bution because of its unique evolutionary history and
biogeography so significantly as the accumulating data particular ecológica! requirements, it is possible to deter-
on píate tectonics beginning in the early 1960s. Most mine patterns (generalized tracks) of coincident distri-
syntheses of historical biogeography before the late 1960s butions of many monophyletic groups. This is the first
were influenced by the arguments of Matthew (1915) step in biogeographic analysis. Second, it is necessary to
that the evolution and distribution of mammals could be determine disjunct clusters of distributions within the overall
explained adequately by continental isostasy. Among distribution of an inclusive taxonomic unit. These clusters
Matthew's many influential disciples was Noble, who, in commonly define the geographic limits of major modern
a series of papers culminating in his synthesis of amphib- biotas, have a high degree of endemism, and constitute
ian biology (1931b), attempted to explain the distribution centers of adaptive radiation. Third, it is desirable to iden-
of families of amphibians by dispersal between static con- tify the historical source units that contributed to the
tinents. With the advent of extensive geophysical evi- modern biotas, for the biota in any given región may
dence in support of continental drift, biogeographers be- have been derived from several historical source units at
gan to reexamine earlier biogeographic arrangements. different times.
The results have been striking changes in biogeographic A major revitalization of historical biogeography has
interpretations. taken place in recent years with the formulation of vi-
In order to address the biogeographic problems, one cariance biogeography (see G. Nelson and Platnick, 1981,
must formúlate working principies and review the geo- and G. Nelson and D. Rosen, 1981, for reviews). Con-
logic and climatic changes that have taken place since siderable controversy exists between adherents of the
the time of the origin of amphibians. This chapter dis- dispersal theory and the proponents of the vicariance
cusses these subjects and then analyzes the historical and theory, who argüe that the vicariance approach provides
modern distributions of the three living orders of am- testable hypotheses, whereas the dispersalist approach is
phibians. untestable. J. Savage (1982) took a balanced view and
outlined the conceptual framework of each approach, as
given below.
BIOGEOGRAPHIC PRINCIPLES
The documentation of the distribution of organisms in Dispersal Theory
space and time is the raw material for biogeographic 1. A monophyletic group arises at a center of or-
analysis. Although each taxon has its individual distri- igin.
477
EVOLUTION
478 2. Each group disperses from this center. mented and the geographically associated taxa in each
3. A generalizad track corresponds to a dispersal fragment evolved together.
route. The major patterns of amphibian distribution at the
4. Each modern biota represents an assemblage familial and subfamilial levéis can be explained best by
derived from one to several historical source vicariance biogeography. Some facets of peripheral dis-
units. tributions definitely are the result of dispersal, but tríese
5. Direction of dispersal may be deduced from are relatívely minor in comparison with the overall dis-
tracks, evolutionary relationships, and past tribution patterns, except for some widespread genera,
geologic and climatic history. such as Bu/o, Hyla, and Rana, in which both phenomena
6. Climatic and/or physiographic change provides seem to have been important. Any biogeographic sce-
the major ímpetus and/or opportunity for dis- nario is only as good as the understanding of the phy-
persal. logenetic relationships of the organisms involved. Unre-
7. Biotas are constituted by dispersal across bar- solved phylogenetic relationships of many amphibian
riers and subsequent evolutíon in isolation. groups, especially some anurans, make some aspects of
8. Dispersal is the key to explain modern pat- the biogeographic analysis tenuous at best.
terns; related groups separated by barriere have Ideally, all biogeographic syntheses should be based
dispersed across them when the barriers were on phylogenetic analyses of componen! taxa. This has
absent or relatívely ineffective, or less com- not been the case, ñor is it likely that this ever will be a
monly by passing over or through existing reality. Instead, the methodology suggested by J. Savage
barriers. (1982) has been used to a great extent, especially with
9. Dispersal is of primary significancc in under- the anurans. This method uses events in the history of
standing current patterns; dispersal preceded the earth to predict general patterns of phylogenetic re-
barrier formation and vicariance, and occurs lationship. This approach implies a reciprocal relationship
again when barriers subsequently are re- between the history of the earth and the history of the
moved or become ineffective. biota.
However, even this approach presents some problems,
Vicariance Theory especially in the anurans, a group in which familial as-
1. Vicariants (allopatric taxa) arise after barriers signments of many taxa are open to question (see Chap-
sepárate parts of a formerly continuous pop- ter 17). Many assumptions are made in the following
ularion. discussion, and in some cases alternatives are offered.
2. Substantíal numbers of monophyletic groups Moreover, if the scenarios depicted are correct, many
are affected simultaneously by the same vi- groups as now recognized are paraphyletic. These in-
cariating events (geographic barrier forma- clude the families Caeciliidae, Myobatrachidae, Lepto-
tion). dactylidae, Bufonidae, Hylidae, and Ranidae, the subfamily
3. A generalized track estímales the biotic com- Microhylinae, and the genera Eleutherodacfylus, Bufo,
position and geographic distribution of an an- Hyla, and Rana.
cestral biota before it subdivided (vicariated) The application of ümes of divergences of lineages de-
into descendant biotas. rived from biochemical studies provides a data set inde-
4. Vicariance after geographic subdivisión pro- pendent of the phylogenies based on morphology and
duced modern biotas. biogeography based solely on earth history. Although the
5. Each generalized track represents a historie evolutionary clock hypothesis of albumen changes has
source unit. been criticized by some workers (see Chapter 16), the
6. Sympatry of generalized tracks reflects geo- results are encouraging. In most cases in which phylo-
graphic overlap of different biotas owing to genetic analyses and earth history agree, there also is
dispersal. congruence of the molecular data.
7. The primary vicariating events are change in The fossil record and the biochemical information em-
world geography that subdivided ancestral phasize the antiquity of many lineages of lissamphibians.
biotas. As gaps are filled in the fossil record, more molecular
8. Biotas evolve in ¡solation after barriers arise. data accumulated, and more cladistic studies completed,
9. Vicariance is of primary importance in under- the biogeographic picture of amphibians should improve.
standing modern patterns; related groups
separated by barriers were fragmented by the
appearances of barriers. HISTORICAL SETTING
The fossil record of modern groups of amphibians ex-
These two approaches differ mainly in their emphases. tends back to the early Triassic (Table 18-1). Therefore,
In the dispersal model, geographically associated taxa in order to interpret the distributional histories of the liv-
dispersed together so as to form a common pattern. In ing groups, it is necessary to project the hypothesized
the vicariance model, original distributions are frag- phylogenetic relationships of each of the orders (see
 Biogeography
Table 18-1. Major Geologic and Climaüc Events Affectíng the Distribuüon of Amphibians 479
Earliest known
Period appearance of
or epoch" Geologic events Climatic events amphibian families''
Triassic, At Permo-Triassic boundary, east Asia consisted of High-latitude humid belts Protobatrachidae
220 m.y. several sepárate blocks south and east of major separated from tropical humid
Asian continent. Otherwise, most if not all belt by midlatitude arid zones;
conünents united in single land mass—Pangaea. expansión of northern in Late
Triassic.
Jurassic, East Asian blocks unite with Pangaea. Breakup of Contraction of arid zones and Karauridae (U)
190 m.y. Pangaea initiated about 180 m.y. when North expansión of high latítude and Prosirenidae (M)
America and África began to sepárate. By 160 especially tropical humid belts. Leiopelmatídae (L)
m.y., Tethys Sea separated east Laurasia from Discoglossidae (U)
east Gondwanaland; epeiric seas probably Palaeobatrachidae (U)
connected Tethys Sea with North Atlantic and
possibly with East Pacific via Caribbean Basin. At
about 140 m.y., Gondwanaland fragmented into
three major blocks—South América-África,
Antarctica-Australia, Madagascar-India.
Cretaceous, Turgai Sea separated east and west Eurasia. Températe humid zones Sirenidae (U)
135 m.y. Midcontinental Sea separated east and west North discontínuous in high latitudes. Amphiumidae (U)
America 100 to 75 m.y. Kolyma Block united with Tropical and subtropical Scapherpetontidae (U)
Asia 120 m.y. South Atlantic Ocean separated climates dominating most land Batrachosauroididae (U)
South America and África ( ± 100 m.y.). masses; arid zones small and Pipidae (L)
Madagascar separated from Indian-Seychellean discontínuous. Pelobatídae (L)
Píate. New Zealand separated from Australia.
Possible connection between Central and South
America in Late Cretaceous.
Paleocene, Turgai Sea separated east and west Eurasia. Equable tropical and subtropical. Cryptobranchidae
65 m.y. Seychelles separated from Indian Píate. Australia Proteidae
separated from Antárctica. Formatíon of Greater Dicamptodontidae
Antilles. DeGeer passage between Europe and Caeciliidae
North America. Beringia intermittent. Brief con- Rhinophrynidae
nection of South America with Central America. Bufonidae
Hylidae
Eocene, Turgai Sea separated east and west Eurasia. Thule Equable tropical and subtropical. Salamandridae
54 m.y. connection of Europe and North America. Pelodytidae
Beringia intermittent. Myobatrachidae
Oligocene, Turgai Sea subsided. Indian Píate collided with Asia. Polar cooling and latitudinal Ambystomatídae
36 m.y. Japanese Archipelago separated from Asia. zonatíon of climates. Leptodactylidae
Southern edge of Oriental Píate formed proto-East Ranidae
Indies. Beringia intermittent.
Miocene, Australian Píate collided with Oriental Píate. Lesser Contínued cooling; eliminatíon of Plethodontidae
23 m.y. Antilles began to form. África briefly connected tropics in North America and Microhylidae
with Eurasia. Beringia intermittent. Uplift of Andes Eurasia. Expansión of arid
and Sierra Nevada ranges. climates.
Pliocene, South America connected with Central America. Contínued polar cooling,
10 m.y. Beringia submerged. latitudinal zonation, and aridity.
"Time since beginning; m.y. = million years. 6L = lower, M = middle, U = upper.

Chapter 17) on the patterns of changing continental con- Geologic Events. At the Permo-Triassic boundary,
figurations and climates during the past 200 million years. eastern Asia consisted of several sepárate blocks south
The continental configurations used here in reconstruct- and east of the major Asian land mass. Otherwise, most,
ing the biogeography of amphibians were taken from the if not all, continental masses were united into a single
paleogeographic maps prepared by Barron et al. (1981). land mass—Pangaea.
The distribution of paleoclimates was synthesized from
various sources, principally Axelrod (1960) and P. Rob-
inson (1973). All dates are given in millions of years be- Climatic Events. Latitudinal zonation of climates ex-
fore the present (my). isted. A tropical (equatorial) humid zone was bordered
by midlatitude arid belts. Humid températe condiüons
Triassic existed at high latitudes. Toward the end of the Triassic,
The earliest period of the Mesozoic extended from about the northern humid zone expanded westward across cen-
220 to 190 my. tral and western Laurasia.
EVOLUTION
480

Figure 18-1. Paleogeographic maps depicting continental movements. A. Middle Jurassic (160 m.y.).
B. Middle Cretaceous (100 m.y.). Edges of continental crusts are outlined. Shaded áreas are emergent land.
Adapted from Mercator projections of Barron et al. (1981).

Jurassic south. Epeiric seas probably connected the Tethys Sea

The initial breakup of Pangaea was in this period, 190 with the North Atlantic Ocean and possibly, by way of
to 135 my (Fig. 18-1A). the Caribbean Basin, with the eastern Pacific Ocean. Ex-
tensive epeiric seas inundated North America and Eurasia
Geologic Events. At the beginning of the Jurassic the from the Arctic Ocean and Asia from the Tethys Sea. By
east Asían blocks united with Pangaea, the breakup of 140 my, that epeiric sea (now called the Turgai Sea)
which was initiated at about 180 my by the opening of fragmented southern Europe and southwestern Asia into
the North Atlantic Ocean and separation of North Amer- many large islands, and separated Europe from Asia. At
ica from África. One píate (the Kolyma Block) rifted from about 140 my, the breakup of Gondwanaland also was
northwestern North America about 180 my and drifted initiated by fragmentation into three major land masses—
westward. By 160 my, the Tethys Sea separated eastern South América-África, Antarctica-Australia, and Mada-
Laurasia to the north from eastern Gondwanaland to the gascar-Seychelles-India.
 Biogeography
Climatic Events. Climatíc zonatíon became less dis- Climatic Events. The climates throughout most of the 481
tinctive with an expansión of the humid zones, especially Cretaceous were equable and tropical or subtropical.
the tropics, with resulting contraction of mid-latitude arid Températe humid zones were discontinuous in the far
zones. north; arid zones were small and discontinuous.

Cretaceous Cenozoic
This is the longest period in the Mesozoic, 135 to 65 my. During the last 65 my the contínents moved to their present
positions and modern climatíc patterns became estab-
Geologic Events. Epeiric seas fragmented many con- lished.
tinents. Although parts of southern Europe and south-
western Asia were united temporarily with the rest of Geologic Events. The Turgai Sea persisted intermit-
Europe about 120 my, and northern Europe with north- tently throughout the first half of the Cenozoic; contin-
western Asia about 100 my, the Turgai Sea persisted uous land connection between Europe and Asia has per-
throughout the Cretaceous (Fig. 18-1B). The Midconti- sisted since the end of the Eocene, about 35 my (Fig.
nental Sea separated eastern and western North America 18-2). The Seychelles broke off from the Indian conünent
in the mid- to late Cretaceous (100 to 75 my), a time about 64 my, and India conünued its northeastward are
when epeiric seas fragmented northwestern África into at to collide with Asia in the Oligocene (about 35 my). The
least two large islands and separated the western part of colusión resulted in the orogenic uplift of the Himalayas,
Australia from the Antarctic-Australian confinen!. The which in time effectively separated the Indian subconti-
Kolyma Block collided with northeastern Asia about 120 nent from the rest of Asia; an extensive embayment in
my. The South Atlantic Ocean began to form between Assam and Burma provided a barrier between India and
África and South America at about 125 my; during the southeastern Asia for much of the later Cenozoic. The
ensuing 20 my, South America drifted westward, and the land mass now represented by the Japanese Archipelago
Atlantic Ocean became continuous. Volcanic actívity in seems to have broken off from Asia at the Oligocene-
the Central American región may have provided an in- Miocene boundary (23 my). The southern and eastern
termittent land connection between North and South edge of the Oriental Píate became a series of islands in
America (Donnelly, 1985); this probably lasted into the the Oligocene and Miocene. Australia separated from
Paleocene. At about 100 my, Madagascar terminated its Antárctica about 55 my (late Paleocene). The northeast-
northeastward drift, whereas the Seychelles-Indian con- ward are of the Australian Píate resulted in its colusión
tínent contínued driftíng. The separation of the land mass with the Oriental Píate in the Miocene with the conse-
now represented by New Zealand occurred at about 74 quent orogeny of the mountains of New Guinea. South
my. America continued to drift westward and finally estab-

Figure 18-2. Paleogeographic map depicting the arrangement of the contínents in the late Eocene (40
m.y.). Edges of continental crusts are outlined. Shaded áreas are emergent land. Adapted from Mercator
projections of Barron et al. (1981).
EVOLUTION
482 lished contact with the Central American appendage of western edges of the continents; the Andes and Sierra
North America in the Pliocene (3-6 my). Nuclear Central Nevada chains uplifted at various times during the Cen-
America was variously connected and separated from ozoic, and by the time of the major uplifts in the Miocene
North America throughout most of the Cenozoic. The and Pliocene they interrupted moisture-laden onshore
opposing movements of the Caribbean Píate (eastward) winds and created rain shadows to the east. During the
with respect to North America and South America (west- last 2 my, Pleistocene climatic fluctuations resulted in four
ward) resulted in the formation of the Greater Antilles, or more major advances of polar and montane glaciers
perhaps as early as the Cretaceous but certainly by the with concomitant latitudinal and altitudinal shifts in tem-
Paleocene (54—65 my), possibly with a continuous land perature belts and the restriction of humid tropical con-
connection with Central America. Beginning in the Mio- ditions during glacial phases and restrictions of the arid
cene, the Lesser Antilles began to arise as oceanic islands tropics during interglacials.
along the are of the Caribbean Píate to form the chain
of islands between South America and the Greater An-
tilles. África had a restricted connection with Eurasia via
LISSAMPHIBIA
Arabia from the late Miocene (about 8-10 my); with the
The fossil record of early lissamphibians is too poor to
rifting of the Red Sea this is now restricted to the Sinai
provide any meaningful ¡nformation on the early distri-
región. Also in the late Miocene and/or early Pliocene
bution of the group. J. Savage (1973) emphasized that
there was a connection between África and the Iberian
the early history of salamanders was associated with
Península. In the Northern Hemisphere there were two
Laurasia, whereas caecilians and most anurans were re-
intermittent connecüons between Eurasia and North
stricted to Gondwanaland. If P. Robinson's (1973) inter-
America. The Beringia land connection between North
pretation of Permo-Triassic climatic zonation is correct,
America and Asia was intermittent throughout most of
the distribution of lissamphibians at that time may have
the Cenozoic and finally submerged in the Pliocene (3-5
been divided by the midlatitude arid belt that ¡solated
my). In the Paleocene-Eocene (50-60 my), two inter-
prosalamanders in the high-latitude humid zone and pro-
mittent connectíons have been postulated to have existed
caecilians and proanurans in the equatorial humid zone.
between northern Europe and North America (McKenna,
1975)—(1) the DeGeer passage via Spitzbergen, north-
ern Greenland, and Ellesmere Island, and (2) the Thule
route via southern Greenland and Ellesmere Island. CAUDATA
The fossil history of the salamanders extends back to the
Climatic Events. At the beginning of the Cenozoic Middle Jurassic, so the evolutionary geography of these
most of the land masses of the world were under equable amphibians is closely correlated with the breakup of Pan-
or subtropical climates; températe climates existed only gaea, especially Laurasia (essentially all fossil and living
at high latitudes. Beginning in the Oligocene, polar cool- salamanders are associated with Laurasian land masses).
ing brought about a more distinctíve latitudinal zonation Milner (1983) provided a geologically well-documented
of climates with a gradual elimination of tropical condi- model for the biogeography of salamanders, but her phy-
tions and vegetation in North America and Eurasia, and logenetic arrangement is notably different from that pro-
with the restriction of tropical groups to the southern pa- posed here (Chapter 17). Although Milner's emphasis on
leopeninsulas (Malay-Indonesian región of southeastern Laurasian cosmopolitanism of salamanders by the Middle
Asia and Central America) by the Miocene. Concomitant Jurassic is correct, some of the details of the model do
with the restriction of the tropics, there was an expansión not fit the phylogenetic history.
of températe climates into the lower latitudes of North The earliest known fossil salamander is the prosirenid
America and Eurasia. During the northeastward drift of Albanerpeton from the Middle Jurassic of Europe. If the
Australia in the Cenozoic, the continent changed latitu- hypothesized phylogeny of salamanders is correct, the
dinal positions with the consequence that the climate four suborders were extant by the Middle Jurassic. How-
changed from moist températe to arid and semiarid over ever, the fossil record of early salamanders provides only
much of the continent in the latter part of the Cenozoic. limited support for this idea. The Karauroidea is known
Also at this time, most terrestrial life was eliminated from only from the Upper Jurassic of Asia, and the Sirenoidea
Antárctica. From the Miocene onward, there was an ex- and Salamandroidea (other than prosirenids) are un-
pansión of the arid and semiarid climates and vegetation known before the Late Cretaceous. Furthermore, the
over southwestern North America, southwestern Asia, Cryptobranchoidea is unknown before the Paleocene.
western South America, and northern África. The de- Nevertheless, the changing continental configurations and
velopment of arid conditions on western sides of conti- climates in the Mesozoic provide a basis for a biogeo-
nents was caused by cooling of high-latitude oceans and graphic interpretation of the phylogenetic model.
the patterns of cold currents from high to low latitudes If protosalamanders were distributed throughout the
along the west sides of continents. Also tectonic processes northern humid zone at the beginning of the Jurassic, the
of the continental crusts of North and South America earliest fragmentation of Laurasia would have played an
resulted in orogenies producing high mountains along the important role in their early evolution. Moreover, only
 Biogeography
483
OTHERS KAR
-60°

-30°

-0'-

ICR oo
SIR en
•60° — CR SAL
KAR
(SI

-30°—

-0°

-60°- CR SIR
E ce Figure 18-3. Diagrammatic representaron of
KAR CO O
the sequential breakup of Laurasia in the Early
and Middle Jurassic and corresponding
vicariance events of the suborders of
SAL salamanders. Cross-hatched regions have
unsuitable climates for salamanders.
Abbreviations: CR = Cryptobranchoidea, KAR
= Karauroidea, KB = Kolyma Block, SAL =
-0*— Salamandroidea, SIR = Sirenoidea.

the northern fragmentatíon would have affected sala- 3. Fragmentation of Euramerica (150 my) result-
manders, because they were excluded from the middle ing in the Sirenoidea surviving only in eastern
and lower latitudes by the arid midlatitude climates. The North America and the Salamandroidea sur-
combination of continental fragmentation (drift and epeiric viving only in Europe (then completely sep-
seas) and expanding humid climates resulted in a series arated from Asia by the Turgai Sea).
of vicariance events that could have given rise to the four
suborders of salamanders by the Middle Jurassic. These Thus, by the Middle Jurassic, four stocks of salaman-
geological and vicariance events are (Fig. 18-3): ders were present on at least five land masses. From this
point in time, the biogeography of each of the suborders
1. Opening of the North Atlantic Ocean in the can be treated separately.
Early Jurassic (180 my) resultíng in the sepa- The Karauroidea may have existed in parts of Asia east
raüon of ancestral salamanders into two stocks of the Turgai Sea until sometime in the Cenozoic, but
along the northern margins of Asia and Eu- the absence of fossils (other than the type) of this extinct
ramerica. The stock in Asia gave rise to the suborder precludes any definitive biogeographic state-
Karauroidea and the one in Euramerica was ments.
the stock for al! other salamanders. According to the vicariance events that isolated the
2. Separation of the northern part of Euramerica suborders on sepárate continental blocks, the Sirenoidea
by the Midcontinental Sea (160 my) resultíng was widespread east of the Midcontinental Sea in North
in the separation of sirenoids in aquatic hab- America in the Upper Cretaceous and early Cenozoic.
itats in eastern North America and crypto- Presumably, limblessness and aquatic habits evolved early
branchoids and salamandroids in terrestrial in the history of the suborder. Concomitant with the zo-
habitats in western and eastern Euramerica, nation of climates beginning in the Oligocene, the distri-
respectively. Cryptobranchoids also were bution of sirenids became restricted to southeastem North
present on the Kolyma Block, which subse- America.
quently rifted from western North America. Early in its history, the Cryptobranchoidea was re-
EVOLUTION
484 stricted to North America. In the Early Jurassic, crypto- are three groups of salamandrids. Pleurodeles in Europe
branchoids probably resembled hynobiids; such a stock and Ty/ototriíon and Echinotríton in eastern Asia share
remained relatively unchanged on the Kolyma Block as primitíve characters and may represent relicts of a for-
it drifted westward from North America and collided with merly widely distributed group of primitíve salamandrids.
eastern Asia in the Early Cretaceous (120 my), thereby Salamandra and its relatíves are restricted to western Eu-
introducing cryptobranchoids into Asia. This was the an- rasia and presumably never existed east of the Turgai
cestral stock of the hynobiids. These salamanders prob- Sea; Salamandra is known in the fossil record of Europe
ably did not reach their easternmost distribution until the since the late Eocene. The so-called Triturus group is
Himalayan Orogeny and the disappearance of the Turgai holarctíc in distribution. This group underwent its early
Sea in the Oligocene. However, they probably were on differentiation ¡n western Eurasia in the Cenozoic (fossil
the land mass that became the Japanese Archipelago Triturus known as early as the Eocene in Europe) and
before that block separated from Asia in the late Oligo- apparently did not disperse into eastern Eurasia until the
cene or early Miocene. The patterns of distribution of the subsidence of the Turgai Sea at the beginning of the
living hynobiids suggest that lineages were isolated in the Oligocene. This timing is in accordance with this group
mesic montane áreas by continental desiccation in the reaching eastern Asia prior to the separation of the land
middle and late Cenozoic. The cryptobranchoid stock mass that was destined to be the Japanese Archipelago
that remained in North America evolved through arrested and also for the dispersa! of salamandrids into North
development to become oblígate neotenes, the crypto- America via Beringia (the first salamandrid fossils in North
branchids. Presumably, these aquatíc salamanders were America are from the late Oligocene).
widespread throughout North America and Eurasia (via If the cladistíc arrangement of the ambystomatids and
the DeGeer Passage) in the early Cenozoic. Latitudinal plethodontíds is correct, there is no major geologic event
climaüc zonation and continental desiccation in the Cen- that could have separated these groups in North America
ozoic resulted in the distributional relicts of Cryptobran- after the Cretaceous, at which time the ancestral stock
chus in southeastern North America and Ananas in might have been split by the Midcontinental Sea. Am-
southeastern China and Japan. bystomatids do not appear in the fossil record until the
The fragmentatíon of what now is Europe and south- Oligocene, and plethodontids are unknown as fossils prior
western Asia by the Tethys Sea probably resulted in sal- to the Miocene. However, ages of separation of genera
amandroids on several small land masses. Contraction of of plethodontids suggested by immunological distances
midlatitude arid zones in the Late Jurassic and Early Cre- are much older; some are placed in the Paleocene (Max-
taceous would have allowed the expansión of the range son et al., 1979). These data suggest that the separatíon
of salamandroids into North America before the complete of ambystomatids and plethodontids in the Cretaceous
separatíon of Europe and North America in the early is reasonable. Ambystomatids seem to have adapted to
Cenozoic. The stocks of salamandroids that gave rise to subhumid climates better than any other North American
the prosirenid-batrachosauroidid-proteid lineage, to the salamanders. Their major centers of differentiation are in
dicamptodontid-scapherpetontid lineage, and possibly to southeastern North America and along the southern edge
the amphiumids must have differentíated prior to the Late of the Mexican Plateau.
Cretaceous. All of these families are known from late The evolution of the plethodontids seems to have been
Mesozoic or early Cenozoic deposits in both Europe and associated with the Appalachian uplands of eastern North
North America, except amphiumids and scapherpeton- America. Generic differentiatíon between Plethodon and
tids, which are known only from North America. There- Ensatina took place in the Paleocene, and differentiatíon
fore, the differentiation of these lineages of salaman- between the eastern and western groups of Plethodon
droids seems to be associated with the complex occurred in the Eocene (dating based on immunological
fragmentatíon of Euramerica in the Middle Jurassic. distances given by Maxson et al., 1979). Presumably
The prosirenids, batrachosauroidids, and scapherpe- Plethodon became separated into eastern and western
tontids are extinct. Proteids survive as the subterranean groups as the result of climatic desiccation in midconti-
Proteus in southem Europe and as five species of Nec- nental North America beginning in the Oligocene. The
turus in eastern North America. The only living dicamp- dispersal of the plethodontid genus Hydromantes from
todonüds are Dicamptodon and Rhyacotriton living in North America to Eurasia presumably took place via Ber-
cold streams in northwestern North America. The only ingia in the Oligocene; dating is based on immunological
surviving amphiumid is Amphiuma in southeastern North data (D. Wake et al., 1979). On the basis of that dating,
America. All of these living salamanders are relicts of it can be assumed that plethodontines of the tribe Boli-
formerly more diverse and widespread groups of sala- toglossini evolved prior to the Oligocene.
manders. The vicariance of the salamandrid and the am- The supergenus Bolitoglossa contains 11 genera and
bystomatíd-plethodontid lineage also may have occurred 140 species in the tropical lowlands and the mountains
toward the end of the Mesozoic, when the last major land of México and Central America; two genera (Bolitoglossa
connections between Europe and North America were and Oedipina) have representativos in South America
broken. According to Ózeti and D. Wake (1969), there (see sectíon: Inter-American Interchange under Anura).
 Biogeography
According to dates suggested by genic differentíation, India and on the Seychelles. But why are there no cae- 485
Bolitoglossa entered South America in the late Miocene, cilians on Madagascar?
prior to the establishment of the present continuous land The spread of ichthyophiids into southeastern Asia and
connection in the Pliocene (Hanken and D. Wake, 1982). adjacent islands must have occurred after the colusión of
The greatest differentiation of genera of bolitoglossines is the Indian Píate with Asia in Oligocene. Some caeciliids
in the mountains of southern México, and the greatest (Dermophis and Gymnopis) dispersed from South Amer-
differentiation of species is in the highlands of south- ica into Central America during a brief connection in the
eastern México (Oaxaca and Veracruz) and nuclear Cen- Paleocene. Others (e.g., Caecilia and Oscaecilia) dis-
tral America (Guatemala and Chiapas, México) and the persed northward only after the closure of the Panama-
highlands of Costa Rica and adjacent Panamá (D. Wake nian Portal in the Pliocene.
and J. F. Lynch, 1976; D. Wake and P. Elias, 1983). This hypothesized history of caecilians is supported (in
It might be expected that the differentiation of bolito- part) by immunological data (Case and M. Wake, 1977).
glossines in México and Central America occurred in as- An estimated divergence üme of Dermophis from Cae-
sociation with the orogenic events that took place prin- cilia of 57 my coincides with the Paleocene separation of
cipally in the Miocene and Pliocene. Immunological South and Central America. Estimated times of diver-
distances provide possible dates for differentiation of spe- gence of African (Boulengerula and Geotrypetes) and
cies of Pseudoeurycea from the Eocene to the Pliocene neotropical (Dermophis) caeciliids of 99 and 120 my are
(8—50 my); differentiation of the genera Chiropterotriton, consistent with the separation of África and South Amer-
Dendrotriton, and Pseudoeurycea occurred in the Paleo- ica. An immunological distance of 210 units between
cene and Eocene according to immunological data (Max- ¡chthyophis and Dermophis suggests an ancient separa-
son and D. Wake, 1981). tion of these taxa, but the limits of accurate measurement
of immunological distance is at about 200 units. Thus it
is possible to suggest only that divergence occured more
GYMNOPHIONA than 120 my.
With the exception of a few caeciliids in Central America
and México and a few ichthyophiids in southeastern Asia,
all living caecilians occur on Gondwanan land masses. ANURA
Moreover, the single fossil caecilian is from the Paleocene J. Savage (1973) provided a lengthy discussion of the
of Brazil. Therefore, the evolutionary history of caecilians distribution of anurans, in which he showed that the his-
must be associated with the history of the southern con- tories of the family groups were intimately associated with
tinents. the histories of the land masses that they occupied in the
If the phylogeny proposed here (Fig. 17-2) is correct, Mesozoic and Cenozoic. In some cases, Savage took un-
the major vicariance events of the families of caecilians warranted liberties with the classification of anurans. For
must have occurred prior to the breakup of Gondwana- example, he eliminated the distributional enigma of a
land. The most primitive caecilians, the rhinatrematíds, dyscophine microhylid in the Oriental Región by assign-
presently are restricted to the northern Andes and Guiana ing the genus Calluela to the Asterophryinae; otherwise,
Shield in South America. Presumably rhinatrematids are the Dyscophinae is restricted to Madagascar. Also, he
relicts of a group that was widespread in Gondwanaland split the melanobatrachine microhylids and placed Mel-
prior to the breakup of the continents in the Late Jurassic. anobatrachus in the Microhylinae and recognized the Af-
Also, the ichthyophiids that survived on the Indian Píate rican genera in the Hoplophryninae. Moreover, he con-
as it drifted from África to Asia are relicts of a formerly sidered the Australo-Papuan hylids to be a sepárate family,
more widely distributed group. Possibly the uraeotyphlids the Pelodryadidae, having a history independent from
and scolecomorphids evolved in situ in peninsular India the neotropical Hylidae. Savage's rearrangements make
and tropical África, respectively. The caeciliids have a perfectly good sense biogeographically, and he may be
classic Gondwanan pattern—South America, África, and correct evolutionarily; existing phylogenetic evidence nei-
India, including the Seychelles Islands. The aquatic ty- ther supports ñor refutes his changes. Savage's phylo-
phlonectids presumably evolved in situ in South America geny of the suborders of anurans was based on P. Star-
from a caeciliid-like ancestor. rett's (1973) suggestion that the pipoid and microhyloid
The distributional data, in combination with the phy- frogs were primitive sister groups. This idea was based
logenetíc arrangement of caecilians, díctate an early di- on her interpretation of the evolution of larval characters.
vergence of most of the families—prior to the Late Ju- Starrett's phylogeny has been disputed by evidence from
rassic, except for typhlonectids. The drift of the Indian larvae provided by Sokol (1975) and Wassersug (1984).
Píate must have carried ichthyophiids, uraeotyphlids, and As emphasized by J. Savage (1973), the historical bio-
caeciliids to Asia; of these, only the ichthyophiids have geography of anurans is associated mainly with Gond-
extended beyond the Indian subcontinent. The presence wanaland. However, limited fossil evidence and present
of caeciliids on the India-Madagascar-Seychelles Píate is distributions of some families of anurans indícate that
obvious because of their presence today in peninsular differentiation of some anuran stocks was associated with
EVOLUTION
486 tne jnitial breakup of Pangaea in the Early Jurassic of South America, and various Cenozoic ages in África
(160-180 my). The Triassic Tríadobatrachus from Mad- and South America; living pipids occur in tropical South
agascar generally is considered to be an early frog. The America and sub-Saharan África.
earliest known fossil that unquesüonably is a frog is Vi- Protopipoids apparently were widely distributed in the
eraella from the Lower Jurassic of Argentina. By the Late humid tropical zone in Pangaea. The vicariance of rhi-
Jurassic there are diverse anuran fossils from Europe, nophrynids from other pipoids may have resulted from
North America, and South America, so it may be as- their isolation in North America after the initial opening
sumed that frogs became widespread in the world during of the North Atlantic Ocean in the early Jurassic (180
the Jurassic. my). Subsequently, the vicariance of palaeobatrachids
Leiopelmatids generally are considered to be the most and pipids could have been associated with the separa-
primitive living anurans. The Jurassic Vieraella and No- tion of western Laurasia from western Gondwanaland by
tobatrachus in Argentina and the living Ascaphus in North the Tethys Sea in the mid-Jurassic (160 my). Palaeo-
America and Leiopelma in New Zealand provide evi- batrachids still had access to North America until the
dence that the primitive frogs grouped in the Leiopel- Eocene. In Europe at least, this family seems to have
matídae were widely distributed prior to the breakup of been the Laurasian counterpart to the Gondwanan pip-
Pangaea and that the living genera are relicts of this an- ids. The palaeobatrachids were widespread and diverse
cient group of anurans. The histories of the other families in Europe; their disappearance at the end of the Pliocene
of anurans (with the possible exception of the pipids) are possibly was caused by the cold climates and glaciation
associated with either Laurasia or Gondwanaland. in the Pleistocene. The history of the Pipidae is associated
with the separation of África and South America and is
Laurasia. Laurasian groups include the Discoglossi- discussed in the following section on Gondwanaland.
dae, Palaeobatrachidae, Rhinophrynidae, Pelobatidae, The pelobatoids include the pelobatids (Eopeloba-
and Pelodytidae. tinae, Pelobatinae, and Megophryinae) and the pelody-
Discoglossids presumably were associated with the hu- üds in Laurasia. Estes (1970) considered the eopeloba-
mid températe climates of Laurasia; the earliest fossils of ünes, which are known from the Late Cretaceous of North
the family are from the Late Jurassic of Europe and the America and Asia, to be the most primitíve group. Pe-
Late Cretaceous of North America. Therefore, it seems lobatines are well represented in the fossil record begin-
likely that discóglossids evolved prior to the breakup of ning in the Eocene of Europe and in the Oligocene of
Laurasia in the Jurassic. Discoglossids seem to have di- North America; however, immunological dating of the
versified in Eurasia west of the Turgai Sea, where four living European Pelábales and North American Scaphio-
genera survive. Subsequent to the subsidence of the Tur- pus indicates divergence in the Cretaceous (Sage et al.,
gai Sea in the Oligocene, the European Bambino dis- 1982). Pelodytíds first appear in the mid-Eocene of Eu-
persed eastward. Ages of differentiation of species of rope, where the living Pehdytes survives; they also are
Bombina determined from immunological distances by known from the Miocene of North America, where the
Maxson and Szymura (1979) show that the eastern Asían family is extinct. Living and fossil pelobatines have greatly
species B. orientalis differenüated in the Miocene, whereas enlarged metatarsal tubercles, and living species are fos-
B. bombina and B. variegata are late Pliocene or Pleis- sorial. Eopelobates has only slightly enlarged metatarsal
tocene vicariants. Climaüc deterioration in midconünen- tubercles and may be a grade in the evolution of the
tal Eurasia in the late Cenozoic and/or Pleistocene cli- fossorial pelobatines. Possibly these anurans evolved in
matic fluctuations resulted in great discontinuities in the the Laurasian arid zone and dispersed throughout xeric
distribution of Bombina. However, Barbourula presum- habitáis in Laurasia prior to the separation of North
ably was in Asia, where it became adapted to tropical America and Eurasia in the Early Jurassic and prior to
conditions. As climatic cooling restricted tropical organ- the contraction of the arid zones in the Mid- and Late
isms to the Indo-Malay región, Barbourula survived in Cretaceous. The megophryines inhabit humid tropical and
Borneo and dispersed to the Philippines. subtropical regions in southeastern Asia and adjacent ar-
Assuming that their unique larvae evolved only once, chipelagos, and some taxa in the Himalayas; there are
the pipoids (Rhinophrynidae, Palaeobatrachidae, and no fossils. Presumably they evolved from an eopeloba-
Pipidae) can be considered a natural group. Early fossil üne-like ancestor (Estes, 1970). If pelodytids are a his-
remains exist from Laurasia and Gondwanaland, and pi- torical reality, they must have diverged from propelo-
poids now occur in tropical North America, South Amer- batids prior to the mid-Jurassic; however, there is no
ica, and África. The palaeobatrachids are known from fossil evidence for such an early vicariance.
the uppermost Jurassic through the Pliocene of Europe,
and from the late Cretaceous of North America. Rhino- Gondwanaland. The vicariance of the other family
phrynids are known from the late Paleocene through the groups of anurans is associated primarily with the breakup
Oligocene of North America; the single living species is of Gondwanaland. It is safe to assume that an ancestral
restricted to México and Central America. Pipids are known stock of arciferal anurans was in Gondwanaland prior to
from the Lower Cretaceous of Israel, Upper Cretaceous the separation of that southern land mass from Laurasia
 Biogeography
Table 18-2. Familias of Anurans and Their Association with myobatrachine genera occurred in the mid-Cretaceous 487
Gondwanan Continente in the Late Jurassic (Assa) or Late Cretaceous (Arenophtyne, Geocrinia,
Africa- Madagascar- Australia- Myobatrachus, Paracrinia, Rheobatrachus, and Taudac-
South America Seychelles-India Antárctica tylus from Crinia); Uperoleia presumably diverged from
Leiopelmatidae Myobatrachidae? Leiopelmatidae Crínia in the late Eocene. On the other hand, hylid dif-
Pipidae Bufonidae? Myobatrachidae ferentiation is a Cenozoic phenomenon (Maxson et al.,
Leptodactylidae Microhylidae Hylidae 1982). In this view divergence of the Cychmna-Litoria
Hylidae Ranidae áurea lineage from other Litaría occurred in the late
Bufonidae Hyperoliidae
Microhylidae Rhacophoridae Eocene, and Cyc/orana and the Litaría áurea group vi-
Ranidae cariated in the late Oligocene. Therefore, it is possible
Hyperoliidae that most, if not all, of the autochthonous genera of Aus-
Rhacophoridae tralian frogs, as well as some species groups, were in
existence before Australia made contact with the Oriental
Región.
in the mid-Jurassic. At that time, this group of anurans The Australian Píate contacted the Oriental Píate in the
shared Gondwanaland with leiopelmaüds and pipids. Prior Miocene and caused the complex uplift of New Guinea.
to the initial breakup of Gondwanaland in the late Ju- This contact provided the first opportunity for inter-
rassic (140 my), this ancestral stock differentiated into change of biotas that had been separated for 120 million
three major groups that can be referred to as the bufon- years since the initial fragmentation of Gondwanaland.
oids, ranoids, and microhyloids. The association of dif- At this time, hylids and myobatrachids from Australia be-
ferent lineages of these three major groups with different came associated with Oriental microhylids in New Guinea,
Gondwanan continents necessitates further differentia- and one stock of Papuan hylids evolved into Nycíimysfes.
tion within each group prior to the fragmentation of the Although there have been brief periods of continuous
continents (Table 18-2), The initial breakup of Gond- land connection between New Guinea and Australia via
wanaland resulted in three continental masses; the his- the Torres Strait as recently as the Pleistocene, few Pap-
tories of the anuran faunas associated with each are dis- uan taxa have dispersed southward into Australia. These
cussed separately. include a few species of Nyctimystes, several species of
Antarctica-Australia.—The anuran fauna of the Ant- two genera of microhylids (Cophixalus and Spheno-
arctica-Australian continent definitely was composed of phryne), and one species of fíana.
leiopelmatids and myobatrachids, and probably hylids. Madagascar-Seychelles-Australia.—The anuran fau-
J. Savage (1973) suggested that microhylids reached the na of the Madagascar-Seychelles-Indian continent that
Oriental Región by being on Antartica-Australia. As em- rifted from the rest of Gondwanaland about 140 million
phasized by Tyler (1979), there is no evidence for the years ago contained only tropical groups. Present on this
presence of microhylids in Australia until the late Ceno- continent were ranids, hyperoliids, rhacophorids, and mi-
zoic, when a few species reached northern Australia from crohylids. Myobatrachids also are presumed to have been
New Guinea. If the Australo-Papuan hylids represent a present, and probably bufonids were present. The ranids
lineage independent from the neotropical hylids, the Hy- consisted of ranines and the stock that gave rise to the
lidae (sensu stricto) was not present on Antarctica-Aus- mantellines. The microhylids minimally consisted of mel-
tralia. anobatrachines, microhylines, and a stock, perhaps much
This continent had températe and tropical climates; like living scaphiophrynines, that was to give rise to five
leiopelmatids apparently became restricted to the former subfamilies. If the Eocene Indobatrachus is indeed a
and myobatrachids to the latter. In the Late Cretaceous, myobatrachid, that family must have been represented
the land mass destined to become New Zealand frag- on the continent. Also, the presence of myobatrachids is
mented from the températe part of the continent. Leio- supported by evidence that myobatrachids and sooglos-
pelmatid frogs survived as the only anurans on New Zea- sids are related. J. Savage (1973) suggested that the ra-
land and became extinct on Antarctica-Australia. diation of bufonids in southeastern Asia was a late Cen-
Biochemical evidence suggests that the three species of ozoic event following the dispersal of Bufo into that región
Leiopelma diverged in the Miocene and Pliocene from North America via Beringia. The diversity of bufonid
(Daugherty et al., 1981). Antárctica and Australia split genera (e.g., Ansonia and Pedostibes) in southeastern
apart in the Paleocene (55 my). Antárctica remained in Asia and adjacent islands strongly suggests an earlier ar-
its polar position and beginning in the Oligocene was rival of a bufonid stock. This arrival could have been via
subjected to extreme cold; the extensive polar icecap now the drifting continent. Unfortunately, there is no fossil
conceals the fossils of the former biota. Australia drifted evidence whatsoever. Savage also suggested that rha-
northeastward and late in the Cenozoic became increas- coporids dispersed from África to Madagascar by waifing
ingly arid. and to southeastern Asia by terrestrial dispersal via south-
According to dates derived from immunological data western Asia, and that hyperoliids dispersed from África
(Daugherty and Maxson, 1982), the differentiation of many to Madagascar and the Seychelles. If these groups of
EVOLUTION
488
Eocene

O-« Sooglossíds
Hyperoliids

Scaphiophrynine. Dyscoph¡ne,& Cophyline Microhylids

Rhacophorids. Hyperoliids, Ranine & Mantelline Ranid:

Oligocene
Bufonids
Ranines
Figure 18-4. Sequential tectonic
movements of India and associated Rhacophorids
land masses during the early and Microhylids
middle Cenozoic, showing (top) the
consequent isolation of anuran taxa
on Madagascar and the Seychelles
Islands and (bottom) the dispersa! of
taxa from India to Asia.

anurans were present on the drifting continent, these The Seychelles Islands have a small but significant
independen! long-distance dispersáis are not necessary. anuran fauna. Except for Ptychadena mascariensis, a waif
During its drift from western Gondwanaland, the Mad- from África via Madagascar, the anuran fauna consists of
agascar-Seychelles-Indian continent fragmented. Mada- three species of the endemic family Sooglossidae and the
gascar split away from the rest of the continent in the monotypic hyperoliid genus Tachycnemis. If sooglossids
mid-Cretaceous (100 my) and moved northward to its indeed are related to myobatrachids, as suggested by J.
present posiüon off the coast of África. As the Indian D. Lynch (1973) and Nussbaum (1979b), sooglossids
continent continued in its are toward Asia, the small land can be viewed as isolated relicts, perhaps derivatives of
mass that later became known as the Seychelles Islands an ancient lineage that is represented only by ¡ndobatra-
broke off in the early Paleocene (64 my). India finally chus from the Eocene of India. Most likely the anuran
collided with Asia in the Oligocene (35 my). This drifting fauna of the Seychelles was much more diverse in the
land mass provided transportation for several groups of early Cenozoic than it is now. There is no reason to
Gondwanan anurans to the Oriental Región and resulted assume that microhylines, ranines, and rhacophorids did
in the isolation of various groups of anurans on fragments not exist there; those groups presumably met the fate of
left along its path. many island populations—extinction.
The major part of the anuran fauna of Madagascar When India collided with Asia in the Oligocene, the
consists of Scaphiophrynine, dyscophyne, and cophyline subcon'inent contained Tomopterna (also present today
microhylids, mantelline ranids, rhacophorids, and hyper- in Madagascar and África), Melanobatrachus (other mel-
oliids. Ranines are represented by one species of To- anobatrachine microhylids in África), ranines, rhaco-
moptema, a genus that also has species in África and phorids, bufonids, microhylines, and an ancestor to the
India. With the exception of Tomopterna and the dys- dyscophine Calluela. Once the land connection was ef-
cophine genus Calluela, which occurs in southeastern fected, these groups (with the exception of Tomopterna
Asia and adjacent islands, all of the subfamilies of ranids and Melanobatrachus) dispersed eastward and thence
and microhylids on Madagascar are endemic, as are the southward into the área that fragmented ¡n the late Oli-
rhacophorid genera Ag/yptodacíy/us and Boophis, and gocene and Miocene into the Greater Sunda Islands (Fig.
the hyperoliid genus Heterixalus. The subfamilies en- 18-4). Most of this dispersa! occurred prior to the marine
demic to Madagascar presumably evolved in situ after transgression into the Assam-Burma región in the late
the separation of the island from the rest of the drifting Cenozoic. Bufonids, rhacophorids, and microhylids ap-
continent, which carried with it Tomopterna and an parently waifed to the Philippines, which aróse in the
ancestor to Calluela (Fig. 18-4). Oligocene.
 Biogeography
The ancestral Calluela (Microhylidae) dispersed through were there) became extinct, and the leptodactylid stock 489
this now insular región and differentíated into a stock that survived only as Heleophryne in cool streams in South
gave rise to the Genyophryninae, represented today by África. Prior to the separatíon of the Madagascar-Sey-
the widespread lowland genera Cophixa/us, Oreophryne, chelles-Indian contínent, microhylids in África already had
and Sphenophryne. With the uplift of New Guinea re- differentíated into melanobatrachines and microhylines.
sultíng from the colusión of the Australian Píate with the The former now is restricted to a few taxa in the moun-
southern edge of the Oriental Píate in the Miocene, this tains of East África. The latter differentíated into two lin-
microhylid stock differentíated into the diversity of gen- eages—phrynomerines and brevicipitines, both of which
yophrynine and asterophryine microhylids known there presently are widely distributed in sub-Saharan África.
today. In África, the pipids differenüated into numerous spe-
The early ranines in the Oriental Región proabably cies; today, Hymenochirus and Pseudhymenochirus are
were the stocks that gave rise to two groups of ranids. restricted to tropical West África, whereas the more spe-
One of these differentíated into several Oriental genera ciose genus Xenopus is widespread in sub-Saharan Áf-
(e.g., Amo/ops and Occidozyga) that are distributed on rica. Among the tree frogs, the hyperoliids have differ-
the mainland (some in peninsular India) and in some entiated into an array of 12 genera and nearly 200 species
cases also in the Greater Sunda Islands and the Philip- throughout sub-Saharan África, whereas the rhacophor-
pines. The other group is the so-called platymantine ran- ids survive only as Chiromantis with three species in trop-
ids (Batrachylodes, Ceratobatrachus, Discodeles, Pal- ical África. Bufonids have diversified into a number of
matorappia, and P/atymanfis). This group is widely genera, and the genus Bu/o is represented by many spe-
distributed from the Philippines to Fiji but does not occur cies. The presence of Bu/o in the Paleocene of Brazil
on the mainland; the greatest diversity is in the Solomon indicates that the genus was in existence before the sepa-
Islands. The genus Rana seems to have arrived in the ration of África and South America. Times of divergences
Indo-Malayan región more recently. based on immunological data corrobórate the Creta-
Africa-South America.—The separatíon of South ceous occurrence of Bu/o (Maxson, 1981a); furthermore,
America from África was initiated in the mid-Cretaceous her data indicated that Schismaderma differentiated in
(100 my), but land connections between the continents the Eocene and at least some species of African Bu/o are
may have persisted until 90 million years ago. Prior to Miocene in origin.
the separation of the continents, the anuran fauna con- África is the site of the major radiation of ranids. A
sisted of pipids, bufonids, leptodactylids, and microhylids ranid stock represented by the Astylosterninae is re-
(Fig. 18-5). Additionally, but apparently restricted to the stricted to humid habitáis in tropical West África, and the
African part of the contínent, there were ranids, hyper- Petropedetinae is widespread in sub-Saharan África. Ter-
oliids, and rhacophorids. Assuming that the dendrobatids restrial-breeding arthroleptines and fossorial hemisines
and petropedetine ranids are sister groups, the immediate represen! two adaptíve types in sub-Saharan África. The
ancestor of these groups must have been present before African ranines are highly diversified in nine genera, of
the separatíon of the continents. Also, if the Australo- which only Rana, Ptychadena, and Tomoptema occur
Papuan hylids are confamilial with the neorropical hylids, outside of África.
the Hylidae would have had to be present at least in the Climatíc deterioration in the latter part of the Cenozoic
South American part of the continent. made much of África uninhabitable for many kinds of
Once South America and África were separated, the anurans. Humid forest refugia persisted in some lowland
anuran faunas diversified independently on the two con- áreas in West África and on ancient mountain masses;
tinents. In África, the leiopelmatids (and hylids, if they many anurans survived the vicissitudes of the Pleistocene

Early Late

/Pipids
Pipids Leptodactylids fHeleophrynids
Leptodactylids \Bufonids ^Bufonids,/
Bufonids ^Hyhd 'Ranids (
Microhylids Microhylines,/ ÍRhacophorids
'Hyperolijds Figure 18-5. Separation of South
America and África in the
iBrevicipitmes Cretaceous. Taxa of anurans Usted
are those presumed to have
inhabited the major part of each
continent.
EVOLUTION
490 in such refugia. These include bufonids such as Necto- During the Cenozoic, the humid températe regions and
phrynoides, hyperolüds such as Chrysobatrachus, and humid tropical regions contracted because of climatic
microhylids such as Hoplophryne. zonatíon. The elevation of the Andes interrupted wind
In South America, the leiopelmatids became extinct. currents and modified patterns of rainfall. The ancient
Several genera of pipids were extant in South America highland áreas—the Brazilian and Guianan shields—
in the Cretaceous and Paleocene, including Xenopus harbor presumed relicts of primitive groups (e.g., Bra-
(Estes, 1975). Xenopus survives only in África, and the chycephalus and elosiines in Brazil, and Oreophrynella
only living pipids in South America are members of the and Otophryne in the Guianas). Late Terüary and Qua-
genus Pipa. The major radiatíons among South American ternary climatic changes are thought to have resulted in
anurans took place in the leptodactylids and hylids. the contractíon of lowland rainforests during arid phases
Primitive leptodactylids, the telmatobiines, diversified correlated with glacial stages in the Pleistocene and con-
in the southern, humid températe región, where many traction of non-forest habitats during humid phases cor-
primiüve telmatobiine genera (e.g., Caudiverbera and related with interglacial stages. These changing condi-
Eupsophus) survive, as does an apparent early deriva- tions, together with correlated altitudinal fluctuations in
tíve, the Rhinodermatidae. Other lineages of leptodac- climate, are responsible for many of the distributional
tylids differentiated and dispersed throughout South patterns existing in South America. Also, patterns of spe-
America. These are recognized now as ceratophryines ciation in some groups of anurans can be associated with
and leptodactylines; the latter are especially diverse in Pleistocene refugia (Duellman, 1982a, 1982b), but the
the tropical lowlands east of the Andes. The hylodines speciation of other groups is much older (Heyer and
are associated with the Brazilian Shield. The largest group Maxson, 1982).
of leptodactylids is the Telmatobiinae, which occurs Determination of the time of differentiation by immu-
throughout the tropical and subtropical parts of the con- nological distances suggests that many leptodactylid gen-
tinent, as well as in the humid températe región. This era (e.g., Caudiverbera, Ceratophrys, Cychramphus,
subfamily contains diverse genera, such as the stream- Leptodacfylus, Odontophrynus, Proceratophrys, Telma-
dwelling Telmatobius in the Andes and the extremely tobius, and Thoropa) date back at least to the Eocene
speciose genus Eleutherodactylus that occurs throughout (Maxson and Heyer, 1982). Furthermore, speciation in
the humid tropical parí of the conünent. many leptodactylids, especially those associated with the
The Hylidae is of unknown origin. Whether the Aus- Brazilian Shield, took place in the Paleocene to Miocene
tralo-Papuan hylids are closely related or the neotropical (Heyer and Maxson, 1982); also, many of the species in
hylids evolved independently from a leptodactylid-like the widespread lowland genus Leptodactylus date from
ancestor in South America, the family underwent a tre- the Eocene. The differentiation among some genera of
mendous radiation in South America. Fossil hylids are hylids seems to have occurred as long ago as the Late
known from the Paleocene of Brazil, but probably before Cretaceous or early Cenozoic. For example, Cryptoba-
the Late Cretaceous three lineages had differentiated— trachus in the northern Andes and Stefania in the Guiana
the arboreal forest-dwelling phyllomedusines, the egg- Shield were estimated to have diverged ¡n the Late Cre-
brooding hemiphractines, and the more generalized hy- taceous (Duellman and Hoogmoed, 1984), and some
lines. Presumably even earlier, two other groups with lowland species of Gastrotheca differentiated in the Pa-
intercalan/ elements evolved from a prohylid ancestor; of leocene or Eocene (Scanlan et al., 1980), as did some
these, the pseudids evolved into a specialized lowland groups oí Bufo (Maxson, 1984). On the other hand, spe-
aquatic group, and the centrolenids into a principally ciation in some oíd genera is relatively recent. For ex-
montane, arboreal group. Maxson's (1976) historical in- ample, Andean species of Telmatobius differentiated in
terpretation of immunological data supports an Early the Miocene to the Pleistocene (Maxson and Heyer, 1982).
Cretaceous divergence of the neotropical subfamilies of Similar recent dates of speciation were determined for
hylids; her limited data also indicated smaller immuno- Andean species of Gastrotheca (Scanlan et al., 1980).
logical distances between neotropical hylines and Aus- Although representing relatively few taxa, the immuno-
tralo-Papuan hylids than between neotropical phyllo- logical data strongly suggest that many of the genera and
medusines and hemiphractines. some of the species of South American anurans evolved
Within South America, the Bufonidae evolved into early in the Cenozoic.
various lineages of Bufo and some specialized, principally Inter-American Interchange.—The complex history
montane groups, recognized as sepárate genera (e.g., of the Central American isthmus and the West Indias has
Atelopus and Oreophrynelh). One presumed derivative received considerable attention from biogeographers. J.
of a bufonid stock, the Brachycephalidae, survives as two Savage (1982) provided a detailed analysis of the Central
monotypic genera in the forests of eastern Brazil. Micro- American herpetofauna. He proposed that a brief Late
hylines diversified into numerous genera and species; they Cretaceous and/or early Paleocene connection between
are distributed throughout tropical South America. the Central American appendage of North America and
The dendrobatids are widespread in South America South America allowed for the dispersal of taxa from one
but are especially speciose in the northwestern part of continent to another. There is no evidence for any North
the continent, where all four genera occur. American amphibians having dispersed to South America
 Biogeography
in the Paleocene, but several groups dispersed northward 491
(Fig. 18-6). These include caecilians, phyllomedusine hy- Late Cretaceous-
lids (ancestral stock of Agalychnis and Pachymedusa), Early Paleocene
microhylines (ancestral stock of Gastrophryne and Hy-
popachus), two stocks oí Bufo, at least one stock of hylids
(including Hy/a), and at least one stock of leptodactylids
(including Eleutherodactylus).
These Paleocene entrants into Central America were
the stocks that evolved into several Mesoamerican groups Caecilüds-x
of Hy/a, Bufo, and Eleutherodactylus, plus many en- Leptodactylids
demic genera (e.g., Crepidophryrte, Plectrohyla, Trí- Bufonids ^
prion, and the eleutherodactyline derivatives—Hylacto- Hylids & Microhylids
phryne, Syrrhophus, and Tomodactylus). Moreover, some Ambystomatid^
of these stocks presumably were associated with the for- Rhinophrynids' Eocene-Miocene
mation of the Greater Antilles, where hylids are respre-
sented by three lineages of Hy/a, plus Osteopilus and Leptodactylids
Calyptahyla. Bufonids & Hylids
Some West Indian Eleutherodactylus (including the
Cuban Smmthillus) seem to have been derived from
Central American groups, whereas others apparently
represen! the evolutionary results of the dispersal of
Eleutherodactylus from South America via the Lesser
Antilles to the Greater Antilles. The Bufonidae is repre-
sented in the Greater Antilles by the endemic Pe/to-
phryne (8 species), which may have been derived from
a Central American bufonid stock. Late Pliocene
The Paleocene separation of North American and South
American stocks of some hylids is supported by immu-
nological data, which used as an evolutionary clock, in-
dícate times of divergence of Agalychnis from Phyllo-
medusa to have been no later than the Late Cretaceous
(Maxson, 1976) and groups of North and South Amer-
ican Hy/a to have been in the Paleocene (Maxson and
A. Wilson, 1975). Moreover, distances between the West
Centrolenids
Indian hylid Osteopilus septentrionalis and various North Dendrobatids & Pipíds
American hylids indícate a divergence in the Paleocene
(Maxson and A. Wilson, 1975). Figure 18-6. Dispersal of families of amphibians between North
With the closure of the Panamanian Portal in the Pli- America, Central America, South America, and the West Indies
from the Late Cretaceous through the Pliocene.
ocene, a great interchange of South American and Cen-
tral American taxa took place. Principal groups of anu-
rans that dispersed northward include some Eleuthero- tral America, southern México, and the West Indies, and
dactylus, Leptodactylus, Physalaemus, Atelopus, some the Gondwanan groups that occur in the Oriental tropics,
Bufo, dendrobatids, centrolenids, some Hy/a, Phryno- there are only three genera of anurans that are Gond-
hyas, and Phyllomedusa. Some South American taxa wanan in origin and widely distributed in the northern
have dispersed no farther than Panamá; this may be the continents. Three other genera of hylids are endemic to
result of either temporal or ecológica! limitaüons. In- North America.
cluded in this group are Pipa, Pleurodema, Rhampho- Bufo presumably was extant before South America
phryne, Gastrotheca, Hemiphractus, Chiasmocleis, and separated from África, and there is evidence that there
Relictivomer. At the same time, some Central American was dispersal of South American Bufo back to África
groups dispersed into South America. Some genera (e.g., toward the end of the connection (Maxson, 1984). Sub-
the hylids Agalychnis and Smilisca) dispersed only into sequently, at least two stocks of Bufo entered North
the northwestern part of the continent. Rana seems to America from South America in the Paleocene. These
be a recent invader from North America; it is represented dispersed into Eurasia via Beringia. The first of these was
in South America by a species that also occurs in Central a tropical group that probably entered Eurasia in the
America. Eocene and had a secondary radiaüon in southern Asia.
The second was a temperate-adapted group that crossed
Laurasian Dispersal of Gondwanan Groups. With Beringia in the Oligocene and became holarctic in distri-
the exception of South American taxa that occur in Cen- bution.
EVOLUTION
492 Tree frOgS of the genus Hy/a also dispersed from South ingia. At least one invasión occurred prior to the late
America to North America in the Paleocene; they appear Miocene, when Rana first appears in the fossil record of
in the North American fossil record in the Oligocene. In North America. Southward dispersal of Rana is limited.
North America, the hylid stock differentiated into a num- Only one species reaches South America, and only one
ber of species, some of which are recognized as different reaches Australia. During the late Miocene and early Pli-
genera—Acris, Limnaoedus, and Pseudacris. A temper- ocene when a land connection existed between north-
ate-adapted Hy/a crossed Beringia probably in the Oli- western África and the Iberian Península of Europe, Rana
gocene; the earliest Eurasian fossil Hy/a are from the was able to disperse southward into mesic habitats in
Miocene of Europe. From this species, the Hy/a arbórea North África.
group of species evolved in températe habitáis in Asia Timing of divergence of some lineages of holarctic Rana
and Europe. Dating of times of divergence from immu- has been determined from immunological data. Uzzell
nological data shows the differentiatíon of hylids in North (1982) noted that several European species of Rana dif-
America to be a Cenozoic phenomenon and the diver- ferentíated in the Oligocene and Miocene (15-35 my).
gence of the Eurasian Hy/a arbórea from North American Divergence of the North American R. catesbeiana group
hylids to be no less than 28 my in the Oligocene (Maxson from the Eurasian R. temporaria complex was in the Oli-
and A. Wilson, 1975). gocene, and times of separatíon of the western North
J. Savage (1973) suggested that Rana invaded Europe American R. boy/ii complex from the Eurasian R. tem-
from África in the early Tertiary. However, after the for- poraria complex vary from 33 to 17 million years (Oli-
mation of the Tethys Sea in the Jurassic, África was not gocene and Miocene) (Post and Uzzell, 1981). Immu-
connected with Eurasia untíl the end of the Miocene. nological distances between the European R. perezi and
Rana is known in the fossil record from the Oligocene the North African R. saharica indícate a divergence time
through the Pleistocene of Europe. Therefore, it seems of about 7 million years, which is in accord with the time
more likely that the ranine stock that reached Asia via of the land connection between those continents (Uzzell,
driftíng India was the source for the non-African members 1982). These data are not overly informative, but they
of the genus Rana. Beginning in the Oligocene, Rana do not refute the hypothesis of an Asian origin of holarctic
dispersed and differentiated. Probably at least two stocks Rana.
of Rana dispersed from Asia to North America via Ber-
 CHAPTER 19
The time has come to rid ourselves ofthe
empírica/ methods which have necessarily
prevailed so long in zoolayy, and endeavor
to group species as far as possible,
according to their phylogenetic
relationships.
George A. Boulenger (19ZOÍ
f Classification

k
> ollowing is a classification of lissamphibians. In each The characters used in the definitions of the families
account of an order, suborder, or family, information is are drawn from the character-state matrices in Chapter
provided in a hierarchical manner; that is, all statements 17. All generic ñames, including synonyms, are usted in
in an ordinal account apply to all suborders and families the Index.
in that order. Within each account, there is a definition
containing a distinctive suite of morphological characters Class AMPHIBIA Linnaeus, 1758
followed by a general description. The morphological Definition.—Amphibians are ectothermic, gnathos-
characters of adults are described in detail in Chapters tome vertebrales having two pairs of limbs (lost in some
13 and 14, and those of larvae are treated in Chapter groups). The skull is characterized by a closed otic notch,
ó.Subsequent sections in each account deal with distri- a large squamosal usually articulaüng with the parietal,
button, fossil history, and life history. In the Remarks post-temporal fossa and ectopterygoid absent, and sep-
section, comments are made about the classification and tomaxilla (if present) internal. The mandible is composed
relationships of the group under discussion. Under Con- of a single coronoid medially and three dermal elements
tent, the numbers of taxa at all levéis down to the species laterally. The skull articúlales with the vertebral column
are given. In the accounts of the families, all genera that by means of a specialized vertebra, the atlas. This ver-
are recognized currently are Usted in alphabetical order tebra lacks ribs and has a pair of atlantal cotyles that
(alphabetically within subfamilies in those families in which articúlate with a pair of medially directed occipital con-
subfamilies are recognized). Each generic listing contains dyles of the skull (one condyle in some Paleozoic am-
generic synonyms (including preoccupied sénior syno- phibians). The lepospondylous (husk-type) vertebrae are
nyms but excluding emendations) in parentheses, fol- composed primarily of membrane bone. The centra are
lowed by the number of species, geographic and geo- elongate with attached, interlocking neural arches; hae-
logical distribution, and a reference to the most recent, mal arches (if present) are fused to the centra. Each ver-
comprehensive treatment of the genus or the most recent tebra bears a pair of projections on each side for the
publication that provides an entree into the pertínent lit- attachment of bicapitate ribs (ribs absent or attached to
erature. The recognized living genera and number of spe- transverse processes in anurans). Lungs are present (sec-
cies follow D. Frost (1985). Ñames of extinct taxa and ondarily absent in some salamanders), and the heart has
synonyms based on fossils are preceded by a dagger (t). three chambers. The skin is glandular and lacks epider-

493
EVOLUTION
494 mai scales, feathers, or hair. The eggs are anamniotic, Order CAUDATA Oppcl, 1811
and aquatic larvae in most groups metamorphose into Definition.—Salamanders have long tails and usually
adult forms. two pairs of limbs of about equal size (hindlimbs absent
Distribution.—Fossil and Recent amphibians have in Sirenidae). Their body form and structure show many
worldwide distributions. At least in the early Mesozoic, similarities to Paleozoic amphibians. An otic notch and
amphibians occurred in Antárctica. Living amphibians are middle ear are absent. The columella has a large foot-
absent from Antárctica and many oceanic islands. plate and short stylus (absent in some taxa). The m. ad-
Fossil history.—Amphibians first appeared in the Early ductor mandibulae internus superficialis originales on the
Devenían; a great radiation took place in the Carbonif- top and back of the skull (except Kamurus), and the m.
erous, and only the Lissamphibia survived beyond the levator (= adductor) mandibulae posterior is small. Post-
Jurassic. orbital, jugal, quadratojugal (except Karauridae), post-
Remarks.—The classification of the extinct amphibi- frontal, postparietal, tabular, supratemporal, supraoccip-
ans is unresolved. There is little agreement about the ital, basioccipital, and ectopterygoid bones are absent.
recognition of subclasses and orders, even the time-hon- Ribs are present. The aquatic larvae (when present) have
ored Labyrinthodontia (see Gaffney, 1979; Ranchen, true teeth on both jaws, gilí slits, and external gills.
1980; and Gardiner, 1982, for recent discussions). Fur- Distribution.—Salamanders are principally holarctic.
thermore, because the Amphibia, as traditionally defined, Eight living and three extinct families occur in North
is the group of tetrapods that lacks amniote eggs, some America (one living family extends into South America),
systematists (e.g., G. Nelson, 1969; E. Wiley, 1979) re- and five living and three extinct familes occur in Eurasia.
ject the Amphibia as a valid taxon, or restrict it to the Fossil history.—Salamanders are reasonably well
Lissamphibia. However, Gardiner (1983) provided syn- represented in the fossil record beginning in the Upper
apomorphies for the class Amphibia. Jurassic of North America and Eurasia and extending
through the Pleistocene. The fossils were reviewed thor-
Subclass LISSAMPHIBIA Haeckel, 1866 oughly by Estes (1981), who did not include the work
Definition.—The vertebrae are monospondylous (i.e., of Nessov (1981). Three fossils are not assigned to fam-
lacking sepárate intercentra). The ribs (if present) are short ilies:
and do not encircle the body cavity. Postfrontals and
cranial roofing bones posterior to the parietals are absent. 1. tComonecíuroides Hecht and Estes, 1960; 1
The surangular bone is absent in the mandible. The teeth species; Upper Jurassic of Wyoming, U.S.A.
are pedicellate (fang-like in some). A columella and oper- 2. tGa/uerpeíon Estes and Sanchíz, 1982; 1 spe-
culum are present (secondarily absent in some taxa). Pa- cies; Upper Cretaceous of Spain.
pilla amphibiorum are present in the inner ear, and green 3. tHy/aeobaírac/ius Dolió, 1884; 1 species; Lower
rods are present in the retina in taxa having fully func- Cretaceous of Belgium.
tional eyes. Fat bodies are associated with the gonads (as
they are in reptiles). Mucous and granular glands are Life history.—Salamanders have a wide range of
present in the skin, and intermaxillary glands are present courtship patterns. Fertilization is external in the Cryp-
in the buccal cavity. tobranchoidea and presumably in the Sirenoidea. In other
Distribution.—Lissamphibians occur throughout the living Salamanders, internal fertilization is accomplished
tropical and températe parts of the world, except for some without copulation. Males have specialized cloacal glands
oceanic islands, principally in the South Pacific Ocean, that produce gelatinous pyramidal structures, spermato-
and the most extreme deserts. phores, which are capped with sperm. Pernales pick up
Fossil history.—Lissamphibians are known from the the sperm cap in the cloaca, the roof of which is modified
Triassic to the Recent. into a spermatheca, where sperm are stored. Eggs usually
Remarks.—Gardiner (1983) considered temnospon- are fertilized as they pass through the cloaca. Salaman-
dyls to be the sister group of the Lissamphibia on the ders of most families deposit their eggs singly or in clumps
basis of three synapomorphies: (1) skull lacking internasal or strings in water; the eggs hatch into aquatic larvae. All
bone, (2) apical fossa small with vomers meeting pre- members of the families Cryptobranchidae, Sirenidae,
maxillae anteriorly, and (3) teeth labyrinthodont. A fourth Amphiumidae, and Proteidae undergo incomplete meta-
character (infraorbital canal in relation to lacrimal and morphosis; they are oblígate neotenes. Most other sala-
jugal bones) given by Gardiner is not applicable to most manders undergo metamorphosis into terrestrial adults.
living Amphibia because they lack those bones. Also, of Most plethodontids have direct development of terrestrial
the temnospondyls, the Permian dissorophoids share the eggs, and some species of Salamandra and Mertensiella
character of the pedicellate teeth with lissamphibians (Estes, are ovoviviparous or viviparous.
1965; Bolt, 1977). Remarks.—With the exception of the three fossil gen-
Contení.—The subclass is composed of three orders era that have not been allocated to families, the place-
containing all living amphibians. ment of Salamanders in families poses few problems.
 Classification
However, grouping of families into suborders is difficult. curves ventrally and medially from that junction. The teeth 495
The substitute ordinal ñame Urodela, dating from La- are nonpedicellate. The vertebrae are amphicoelous, and
treille, 1825, commonly is used in place of Caudata. all but the first two spinal nerves exit intravertebrally. The
Contení.—Four suborders are recognized provision- ribs are bicapitate, and the ypsiloid cartilage is absent.
ally. In addiüon to the three monotypic fossil genera not Fertilization presumably is external. Sirens have several
assigned to families, these suborders include nine living unique character states among salamanders; these are
and four extinct families containing 62 living genera with (1) nasals ossified from median anlagen; (2) palatal teeth
352 living species. Sixty-seven extinct species are placed in large patches, (3) m. adductor mandibulae internus
in some of the living genera and in 34 extinct genera. superficialis originatíng on side of skull, (4) 46-64 ma-
crochromosomes and no microchromosomes (possibly
Suborder tKARAUROIDEA Estes, 1981 tetraploids), (5) premaxillary teeth absent, replaced by
The oldest known salamander has a unique combinaüon horny beaks, (6) ¡nterventricular septum present, and (7)
of characters (see account of Karauridae for characters glomeruli well developed in anterior part of kidney.
and discussion). Sirenids exhibit several paedomorphic features, such
as the absence of eyelids and presence of gilí slits (one
tKARAURIDAE Ivachnenko, 1978 in Pseudobranchus and three in Siren) and external gills
Deflnition.—A single fossil from the Jurassic is defined (Fig. 19-1). The forelimbs are greatly reduced; Siren has
by a suite of primitive character states. The dorsal processes four digits on each forefoot, Pseudobranchus only three.
of the premaxillae are short and do not sepárate the The bodies are long and slender. Siren lacertma attains
nasals. Lacrimáis and quadratojugals are present. The a length of 950 mm, whereas Pseudobranchus attains a
angular is not fused with the prearticular, and a sepárate length of only 250 mm.
coracoid ossificatíon is absent. The m. levator mandib- Distribución.—Living sirenids are restricted to south-
ulae internus superficialis originales on the skull roof only. eastern United States and northeastern México (Fig. 19-
The teeth are pedicellate, and the palatal dentítion par- 2).
allels the maxillary and premaxillary teeth. The vertebrae
are amphicoelous, and all spinal nerves exit interverte-
brally. The ribs are bicapitate. This small (120-mm snout-
vent length) salamander has a large, flattened skull with
pitted dermal sculpture.
Fossil hístory.—This family is represented by a single
skeleton from the Upper Jurassic of southern Kazakhstan,
U.S.S.R.
Remarks.—Estes (1981) noted the presence of many
primitive characters in this ancient salamander and placed
it in its own suborder.
Contení.—A single monotypic genus:

1. tKaraurus Ivachnenko, 1978; 1 species. Upper

Jurassic, southern Kazakhstan, U.S.S.R.
Figure 19-1. Siren intermedia from Louisiana, U.S.A. Photo by
Suborder SIRENOIDEA Goodrich, 1930 J. T. Collins.
A single family of aquatic, eel-like salamanders consti-
tutes this distinctive suborder (see account of Sirenidae
for characters and discussion).

SIRENIDAE Gray, 1825

Deflnition.—The pelvic girdle and hindlimbs are ab-
sent. The dorsal processes of the premaxillae are short
and do not sepárate the nasals (Fig. 13-3G). Septomax-
illae, coracoids, and second ceratobranchials are present.
Maxillae are absent (Pseudobranchus) or free and eden-
tate (Siren). The pterygoids are reduced, and the angular
is fused with the prearticular. The exoccipital, prootic,
and opisthotic are not fused, and the internal caroüd fora-
men is absent. The columella is free from the operculum. Figure 19-2. Distribution of living memoers of the family
The periotic canal joins the periotic cistern dorsally and Sirenidae.
EVOLUTION
496 Fossil history.—Sirenids are well represented in the per Cretaceous and upper Paleocene of north-
fossil record in North America with one extinct genus, central United States. Estes (1981).
Habrosaurus, in the Upper Cretaceous and Paleocene, 2. Pseudobranchus Gray, 1825 (Paruibranchus
Siren from the Eocene to Recent, and Pseudobranchus Hogg, 1839); 1 species. Southeastern United
from the Pliocene to Recent. States. Pliocene and Pleistocene of Florida,
Life history.—Because a spermatheca is absent in fe- U.S.A. Martof (1972).
males and cloacal glands are absent in males, sperma- 3. Siren Linnaeus, 1766; 2 species. Southeastern
tophores presumably are not produced, and fertilization United States and northeastern México. Mid-
probably is external. The eggs are deposited singly or in dle Eocene of Wyoming, middle Miocene of
small clumps attached to submerged vegetaüon in ponds Texas, lower Miocene and Pleistocene of
and swamps. Florida, U.S.A. Martof (1974).
fíemarfcs.—The relationships of sirenids with other
salamanders is problematical, because sirenids possess Suborder CRYPTOBRANCHOIDEA Dunn,
(1) a number of primitive characters shared with cryp- 1922
tobranchoids, (2) numerous derived characters shared Definition.—The dorsal processes of the premaxillae
with more advanced salamanders, (3) severa! paedo- are short and do not sepárate the nasals, which are os-
morphic characters shared with other neotenic families, sified from two anlagen. The angular is not fused with
and (4) a suite of unique primitive and derived charac- the prearticular. The second ceratobranchials and the yp-
ters. C. Goin and O. Goin (1962) placed sirenids in a siloid cartilage are present. The vertebrae are amphicoe-
sepárate order, Trachystomata, and suggested a relation- lous, and only the posterior caudal vertebrae exit intra-
ship with the lepospondyls; this was rejected by Estes vertebrally. The ribs are unicapitate. Fertilization is extemal.
(1965), whose conclusions were followed by D. Wake The diploid number of chromosomes ¡s 56 or more and
(1966), Edwards (1976), and Hecht and Edwards (1977). consists of a few macrochromosomes and many micro-
Estes (1981) provisionally placed the sirenids and the chromosomes. Cryptobranchoids have two unique struc-
salamandrids together in the Salamandroidea because of tural features—the first hypobranchial and first cerato-
the number of shared derived characters. An analysis of branchial are fused into a single rod, and the m. puboübialis
the character states given in Table 17-1 shows only seven and m. puboischiotibialis are fused.
synapomorphies uniting sirenids and salamandrids; this The Cryptobranchoidea includes two rather different
is equal to the number uniting sirenids and plethodontíds families—the relatively small, terrestrial or mountain-brook
and one less than the number shared by sirenids and hynobiids of Asia and the largest living salamanders, the
proteids and amphiumids. The paedomorphic nature of aquatic cryptobranchids, in North America and Asia.
many of these character states weakens their usefulness Distributíon.—Cryptobranchoids occur in eastern North
in determining phylogenetic relationships. Based on America and in Asia eastward from Irán, Turkestan, and
characters not heavily influenced by paedomorphosis, it the Ural Mountains to China, Korea, and Japan.
seems that sirenids are derived from a basal stock of post- Fossil history.—All fossil Cryptobranchoids are refer-
karauroid salamanders. able to the Cryptobranchidae (see account of family).
Contení.—Six fossil and three living species are placed Life history.—Aquatic eggs masses are enclosed in
in one extinct and rwo living genera: sacs (one from each oviduct) and fertilization is external.
Remarfcs.—The hynobiids and cryptobranchids usu-
1. tHabrosaurus Gilmore, 1928 (tAde/phesiren ally have been grouped together. Although they share
Goin and Auffenberg, 1958); 1 species. Up- mainly plesiomorphic character states (Estes, 1981), their

Figure 19-3. A. Hynobius

retardatus from Japan. B. Ranodon
sibirícus from the Soviet Union.
Photos by J. T. Collins.
 Classification
497

Figure 19-4. Distribution of the

living members of the family
Hynobüdae ¡n Asia and of the family
Ambystomatidae in North America.

association is based on three synapomorphies: (1) fusión phore, and the female deposits eggs on top of it.
of first hypobranchials and first ceratobranchials, (2) fu- Remarks.—The only reviews of the hynobiid sala-
sión of tibialis muscles, and (3) eggs enclosed in paired manders are by E. Dunn (1923), Thom (1968), and Zhao
sacs. and Q. Hu (1984). Tihen (1958), D. Wake (1966), and
Contení.—Two living families, the Hynobüdae and Regal (1966) suggested possible relaüonships with the
Cryptobranchidae, are included in the suborder. Ambystomatoidea, but Edwards (1976) emphasized that
such a relationship was based on symplesiomorphies.
HYNOBIIDAE Cope, 1859 Contení.—Nine genera containing 32 species are rec-
Definition.—Metamorphosis is complete. Adults have ognized:
eyelids and no gilí slits, and larvae have four pairs of gilí
slits. Lacrimáis and septomaxillae are present (Fig. 13- 1. Batrachuperus Boulenger, 1878; 6 species.
3A). The palatal dentition pattern is transverse, not par- Western China, Tibet, Afghanistan, and Irán.
alleling the maxillary and premaxillary teeth. Thorn (1968).
Hynobiids are small to moderate-sized salamanders. 2. Hynobius Tschudi, 1838 (Pseudosa/amandra
Several species of Hynobius attain máximum total lengths Tschudi, 1838; Molge Bonaparte, 1839; Hy-
of no more than 100 mm, whereas Ranodon sibiricus droscopes Gistel, 1848; Ellipsoglossa Duméril
attains a total length of more than 200 mm. Adults of and Bibron, 1854; /sodacfy/um Strauch, 1870;
most genera are terrestrial and have well-developed lungs Turanomo/ge Nikolski, 1918); 17 species. Ja-
(Fig. 19-3), but Onychodacíy/us lives in mountain streams pan; eastern Asia westward to Turkestan,
and has no lungs. Larval hynobiids have external gills U.S.S.R. Thorn (1968); Zhao and Q. Hu
and caudal fins. (1984).
Distribution.—These Asian salamanders range from 3. Liuia Zhao and Hu, 1983; 1 species. North-
Siberia westward to the Ural Mountains and southwest- central China. Zhao and Q. Hu (1983).
ward to Turkestan, Afghanistan, and Irán, and southward 4. Onychodacty/us Tschudi, 1838 (Dacty/onyx
to China, Korea, and Japan (Fig. 19-4). Bibron, 1839; Onychopus Duméril, Bibron,
Fossil history.—No fossils are known. and Duméril, 1854; Geomolge Boulenger,
Life history.—All hynobiids have aquatic eggs and lar- 1886); 2 species. Northeastern Asia; Honshu
vae. The eggs are deposited in two spindle-shaped ge- and Shikoku Islands, Japan. Thorn (1968).
latinous sacs representing the eggs from each oviduct. 5. Pachyhynobius Fei, Hu, and Wu, 1983; 1 spe-
The egg sacs are attached to stones or vegetation and cies. Northeastern China. Zhao and Q. Hu
subsequently are fertilized. Hynobius and some Batra- (1984).
chuperus deposit eggs in ponds; other Batrachuperus, 6. Pachypa/aminus Thompson, 1912; 1 species.
Onychodactylus, and Ranodon deposit eggs in streams. Japan. Thorn (1968).
The larvae of Hynobius hatch at a poorly developed stage 7. Paradacty/odon Risch, 1984; 1 species. North-
and have balancers, whereas those of the stream-breed- central Irán. Risch (1984).
ers hatch at a more advanced stage. Bannikov (1958) 8. fíanodon Kessler, 1866 (Ranidens Boulenger,
reported that Ranodon sibiricus deposits a spermato- 1882; Pseudohynobius Fei and Ye, 1983); 2
EVOLUTION
498 species. Mountains of northern China and ad- Contení.—Two genera contain three living and two
jacent Russia. Zhao and Q. Hu (1984). extinct species:
9. Salamandrella Dybowski, 1870; 1 species.
Russian Turkestan through northern China and 1. Andrias Tschudi, 1837 (tProfeocordy/us Cu-
far eastem U.S.S.R. to Hokkaido, Japan. Zhao vier, in Eichwald, 1831; tPa/aeotriíon Fitzin-
and Q. Hu (1984). ger, 1837; Megalobatrachus Tschudi, 1838;
Sieboldia Gray, 1838; tHydrosa/amandra
CRYPTOBRANCHIDAE Fitzinger, 1826 Leuckart, 1840; tTritogenius Gistel, 1848;
Definition.—Metamorphosis is incomplete. Adults lack tTriíomegas Duméril and Bibron, 1854; Me-
eyelids and have one pair of gilí slits (closed in Andrias). galobranchus Van der Hoeven, 1855; Hoplo-
Lacrimáis and septomaxillae are absent (Fig. 13-3B). The batrachus Mollendorff, 1877; tP//cagna£hus
palatal teeth are in a curved row parallel to the maxillary Cook, 1917; tZaisanurus Tschernov, 1959);
and premaxillary teeth. 2 species. Japan and central China. Upper
These huge, aquaüc salamanders have depressed bod- Oligocene to upper Pliocene of Europe; Mio-
ies and fleshy dermal folds (Fig. 19-5). Andrias dauidi- cene of North America and Pleistocene of Ja-
anus attains a total length of 1520 mm, A. japónicas pan. Liu (1950); Zhao and Q. Hu (1984).
1440 mm, and Cryptobranchus alleganiensis 750 mm. 2. Cryptobranchus Leuckart, 1821 (Urotropis
Larvae have caudal fins and short gills. Rafinesque, 1822; Protonopsis LeConte, 1824;
Distribution.—The range of the family includes east-
ern North America, central China, and Japan (Fig. 19-
6).
Fossil history.—This family is known from the Paleo-
cene, Miocene, and Pleistocene of North America, the
Oligocene through the Pliocene of Europe, and the Pleis-
tocene of Asia. Fossil Andrias attained total lengths of
2300 mm (Estes, 1981).
Life history.—Eggs are laid in paired, rosarylike strings,
one from each oviduct, in depressions beneath stones in
streams; ferülization is external. Several female Crypto-
branchus may use the same nest site, and parental care
of eggs occurs in Andrias.
Remarks.—The cryptobranchids seem to be derived
from a hynobiid-like ancestor through the retention of
larval characters in the adults. Estes (1981) reviewed fos-
sil cryptobranchids and tentatively did not accept Nay-
lor's (1981) placement of Andrias in the synonymy of Figure 19-5. Cryptobranchus alleganiensis from Missouri, U.S.A.
Cryptobranchus. Photo by J. T. Collins.

Figure 19-6. Distribution of living

members of the family
Cryptobranchidae.
 Classification
Abranchus Harían, 1825; Menopoma Harían, mandibular rami with interlocking symphysis, and (4) 499
1825; Salamandrops Wagler, 1830); 1 spe- cervical vertebrae modified to form an atlas-axis-like
cies. Eastern United States. Upper Paleocene complex. These small, elongate salamanders may have
of Saskatchewan, Canadá, and Pleistocene of been aquatic or even fossorial.
Maryland, U.S.A. Nickerson and Mays (1973). Fossil history.—Prosirenids are known from the Mid-
dle Jurassic to the middle Miocene of Europe, the Lower
Suborder SALAMANDROIDEA Noble, 1931 Cretaceous of North America, and the Upper Cretaceous
Definition.—In this suborder, the dorsal processes of of southwestern Asia.
the premaxillae are long and sepárate the nasals, which Remarks.—Because of incomplete specimens, some
ossify from lateral anlagen (nasals absent in proteids). important features cannot be determined. Moreover, there
The angular is fused with the prearticular in living families are some inconsistencies in the diagnostic characters (e.g.,
(not fused in extinct families). The ribs are bicapitate. unicapitate ribs in Albanerpeton, according to Estes, 1981).
Three other characters are shared by the living families, The unique derived characters of prosirenids set them
but their states are unknown in the fossil families: (1) apart from other families of salamanders. Although the
second ceratobranchials absent, (2) diploid chromosome nonpedicellate structure of the teeth is shared with the
number 38 or less and with no more than one pair of Sirenidae, the abundance of characters unique to each
microchromosomes, and (3) ferülization intemal by means family suggest that sirenids and prosirenids are not closely
of spermatophores. related.
Most salamandroids are terrestrial and small to mod- Contení.—Six extinct species are placed in four gen-
érate in size, but the suborder contains two groups of era:
large, neotenic salamanders that lack eyelids and have
persisten! gilí slits. 1. ^Albanerpeton Estes and Hoffstetter, 1976; 3
Distribution.—This suborder occurs throughout the species. Jurassic to Miocene of Europe; Up-
températe holarcüc región and enters the Neotropics into per Cretaceous of North America.
South America. 2. tNufcusurus Nessov, 1981; 1 species. Upper
Fossil history.—An extensive fossil record begins in Cretaceous of Uzbekistán, U.S.S.R.
the Jurassic of Europe and the Cretaceous of North 3. tProsiren Goin and Auffenberg, 1958; 1 spe-
America and western Asia. cies. Lower Cretaceous of Texas, U.S.A.
Life history.—Males have modified cloacal glands for 4. tí?amone//us Nevo and Estes, 1969; 1 species.
the production of spermatophores, and females have a Lower Cretaceous of Israel.
spermatheca for sperm storage; fertilization is internal.
Remarks.—The families herein grouped in the Sala- tBATRACHOSAUROIDIDAE Auffenberg,
mandroidea were placed in six suborders by Estes (1981), 1958
who noted that his placement of several families was Definition.—The premaxillae are paired. The exoccip-
questíonable. The shared derived states of the premax- ital, prootic, and opisthotic are fused, and the internal
illae, nasals, angulars, ribs, ceratobranchials, chromo- carotid foramen is absent. The teeth are pedicellate. The
somes, and fertilization indícate that the salamandroids vertebrae are opisthocoelous (amphicoely secondary in
are monophyletíc. However, the relationships among the Palaeoproteus and Peratosauroides), and all spinal nerves
families included in the suborder are obfuscated by the exit intravertebrally. Among salamanders, batrachosau-
paedomorphic nature of many characters used to sepá- roidids are unique in lacking a tuberculum interglenoid-
rate the families and the absence of information con- eum on the atlas. At least some of these large, paedo-
cerning the characters of many of the extinct families. morphic salamanders had elongate bodies and reduced
The subordinal ñame Amphiumoidea Cope, 1889, an- limbs; probably they were aquatic.
tedates Salamandroidea, but because Amphiumoidea has Fossil history.—Batrachosauroidids are known from
been used only for the Amphiumidae and because the the Upper Cretaceous to the lower Pliocene of North
Law of Priority does not apply to ordinal ñames, the America, from the middle Eocene and possibly the Upper
more commonly used Salamandroidea is employed here. Cretaceous of Europe, and from the Upper Cretaceous
Contení.—Six living and three exünct families com- of southwestern Asia.
prise this suborder. Remarles.—The family seems to be most closely re-
lated to proteids; if the oldest members of the ancestral
tPROSIRENIDAE Estes, 1969 group to proteids and batrachosauroidids were opistho-
Definition.—The premaxillae are paired, and lacrimáis coelous (as indicated by the oldest batrachosauroidid fos-
are present. The exoccipital, prootic, and opisthotic are sils), both proteids and later batrachosauroidids regained
fused, and the internal carotid foramen is absent. The amphicoely. Both families are paedomorphic, but dis-
vertebrae are amphicoelous, and all spinal nerves exit tincüve features (e.g., absence of maxillae in proteids)
intravertebrally. Unique character states of the prosiren- sepárate them. Estes (1981), who reviewed the family,
ids are (1) teeth nonpedicellate, (2) frontals fused, (3) noted the presence of subpedicellate teeth in Palaeopro-
EVOLUTION
500 teus and that the questionable batrachosauroidid fossil body, four digits on all feet, pigmented skin, and small,
from the Late Cretaceous of France was not referred to but normal, eyes.
a genus. Distribution.—The range of the family is disjunct.
Contení.—Eight exünct species are recognized in six Necturus occurs in eastern North America, and Proteus
genera: is restricted to subterranean waters in southeastern Eu-
rope (Fig. 19-8).
1. TBatrachosauroides Taylor and Hesse, 1943; Fossil history.—Although not abundant in the fossil
2 species. Lower Eocene and Miocene of North record, proteids are known from the upper Paleocene
America. and Pleistocene of North America, Miocene and Pleis-
2. tMj/nbu/afcía Nessov, 1981; 2 species. Upper tocene of Europe, and Miocene of Asia.
Cretaceous of Uzbekistán, U.S.S.R. Life history.—Courtship, maüng, and oviposition take
3. tOpisthotriton Auffenberg, 1961; 1 species. place in water (usually streams). The eggs are laid indi-
Upper Cretaceous and Paleocene of North vidually on the undersides of stones.
America. Remarks.—Some workers, principally Hecht and Ed-
4. tPa/aeoproíeus Herré, 1935; 1 species. Middle wards (1977), place Proteus and Necturus in sepárate
Eocene of Germany. families, but most evidence suggests that they are closely
5. tPerafosauroides Naylor, 1981; 1 species. related (see Estes, 1981, for summary and references).
Lower Pliocene of California, U.S.A. Comonecturoídes, formerly placed in the Proteidae, was
6. tProdesmodon Estes, 1964 (Cuííysar/cus Estes, removed by Estes (1981), who recognized the suborder
1964); 1 species. Upper Cretaceous and lower Proteoidea containing the Proteidae and Batrachosau-
Paleocene of North America. roididae.
Contení.—Two genera contain six living species; four
PROTEIDAE Gray, 1825 other species are extinct:
Deflnition.—The premaxillae are paired. Septomaxil-
lae, lacrimáis, ypsiloid cartílage, and the basilaris complex 1. tMíoproíeus Estes and Darevsky, 1978; 1 spe-
of the inner ear are absent. The opisthotic is not fused cies. Middle Miocene of Caucasus Mountains,
with the prootic and exoccipital, and the interna! carotid U.S.S.R.
foramen is present. The teeth are pedicellate, and the 2. Necturus Rafinesque, 1819 (Exobranchia Raf-
palatal teeth parallel the premaxillary teeth. Proteiids are inesque, 1815; Phanerobranchus Leuckart,
unique in having (1) no maxillae, (2) the perioüc canal 1821; Menobranchus Harían, 1825); 5 spe-
horizontal from its posterodorsal junction with the periotic cies. Eastern North America. Paleocene of
cistern, (3) two pairs of larval gilí slits, and (4) a diploid Canadá; Pleistocene of Florida, U.S.A. Hecht
chromosome number of 38. (1958).
These aquatic salamanders have large, filamentous gills 3. tOrt/iop/iyia Meyer, 1845; 1 species. Upper
and caudal fins (Fig. 19-7). Proteus has an elongate, slen- Miocene of Germany.
der body and reduced number of digits (three on fore- 4. Proteus Laurenti, 1768 (Lavaríus Rafinesque,
feet, two on hind feet); in this subterranean salamander, 1815; Platyrhynchus Leuckart, 1816; Hypo-
pigment is absent in the skin, and the eyes are degen- chthon Merrem, 1820; Caledon Goldfuss,
erate. Proteus attains a total length of about 300 mm, 1820; Apneumona Fleming, 1822; Catedon
whereas Necturus reaches 400 mm and has a robust Duméril and Bibron, 1854); 1 species. Car-
niola Alps of Italy and Yugoslavia. Pleistocene
of Germany. Thorn (1968).

DICAMPTODONTIDAE Tihen, 1958

Deflnition.—The premaxillae are paired. Septomaxil-
lae, lacrimáis, and the ypsiloid cartílage are present. The
exoccipital, prootíc, and opisthotíc are not fused, and the
internal carotid foramen is present. The nasals are ossi-
fied from lateral anglagen (nasals reduced or absent in
Rhyacotriton}. The teeth are pedicellate, and the palatal
teeth are in an M-shaped pattern. The columella is free
from the operculum; the pterygoid is reduced in Rhy-
acotriton (Fig. 13-3C). The periotic canal is horizontal
from its junction with a protrusion of the periotic cistern
into the fenestra ovalis (canal flexed in Rhyacotriton).
The vertebrae are amphicoelous, and all postcranial nerves
Figure 19-7. Necturus maculosus from Missouri, U.S.A. Photo by exit intravertebrally. The diploid number of chromo-
J. T. Collins. somes is 26 or 28.
 Classification
501

Figure 19-8. Distribution of living

members of the family Proteiidae in
eastern North America and southern
Europe and of the family
Dicamptodontidae in western North
America.

bystomatidae (Tihen, 1958). Edward's (1976) work on

spinal nerves showed that dicamptodontids have a pat-
tern shared only with the Scapherpetontidae, which along
with other characters (e.g., presence of lacrimáis and free
columella), were regarded by Estes (1981) to be sufficient
to give familia! status to the dicamptodontids. All of the
fossil taxa and the living Dicamptodon are placed in the
subfamily Dicamptodontinae, characterized by: (1) teeth
compressed, bladelike; (2) nasals and pterygoids well de-
veloped; (3) carpal and tarsal elements ossified in adults;
(4) ypsiloid cartilage and lungs well developed; and (5)
diploid chromosome number 28. Rhyacotríton is placed
in its own subfamily, characterized principally by pae-
domorphic states: (1) teeth conical; (2) nasals reduced
or absent and pterygoids reduced; (3) carpal and tarsal
Figure 19-9. Dicamptodon ensatus from Washington, U.S.A.
Photo by J. T. Collins. elements cartilaginous in adults; (4) ypsiloid cartilage and
lungs reduced; and (5) diploid chromosome number 26.
Some workers (e.g., Milner, 1983) have considered Rhy-
These generalized aquatic salamanders have well-de- acotriton to be more closely related to plethodontids.
veloped limbs and eyelids; larvae have four pairs of gilí However, Dicamptodon and Rhyacotríton share patterns
slits and short, nonfilamentous gills (Fig. 19-9). Dicamp- of palatal dentítion and spinal nerves. The similarities be-
todon attains a total length of 351 mm, whereas Rhy- tween Rhyacotríton and plethodontids are the result of
acotríton is small (100 mm). convergence of paedomorphic characters, but the syna-
Distribuí/orí.—Pacific coastal región and mountains of pomorphies grouping Rhyacotriton and Dicamptodon are
northwestern United States from Washington (and ad- weak. The two genera may represent independen! lin-
jacent Canadá) to northern California, and in the north- eages, in which case the Dicamptodontidae is polyphy-
ern Rocky Mountains in Idaho (Fig. 19-8). letic.
Fossil history.—Dicamptodontids are known from the Contení.—Three species in two living genera and five
Paleocene, lower Eocene and Pliocene of northwestern monotypic extinct genera are grouped into two subfam-
United States and from the Paleocene and upper Mio- ilies:
cene of Europe.
Life history.—Eggs are deposited singly either free un- DICAMPTODONTINAE Tihen, 1958
der stones or in cracks, or attached to undersides of stones 1. tAmbystomichnus Peabody, 1954; 1 species.
in cold streams, where they may take up to 9 months to Paleocene of Montana, U.S.A.
hatch. Larvae require 2 to 4.5 years to reach metamor- 2. tBargmannia Herré, 1955; 1 species. Upper
phosis. Miocene of Czechoslovakia.
Remarks.—Untíl recently, the dicamptodontids usu- 3. tChrysotriíon Estes, 1981; 1 species. Lower
ally were regarded as one or two subfamilies of the Am- Eocene of North Dakota, U.S.A.
EVOLUTION
502 4. Dicamptodon Strauch, 1870 (Chondrorus Upper Cretaceous to the lower Eocene of northwestem
Cope, 1887); 2 species. Pacific coast of Cal- United States and Canadá north to Ellesmere Island.
ifornia to Britísh Columbia; northern Idaho, Remarks.—On the basis of their shared pattem of spinal
U.S.A. Lower Pliocene of California. Nuss- nerve foramina (nerves exit via foramina in postsacral
baum (1976). vertebrae and between vertebrae presacrally), Edwards
5. tGeyerie//a Herré, 1950; 1 species. Upper Pa- (1976) placed the scapherpetontíds and dicamptodontíds
leocene of Germany. in a single family. However, Estes (1981) recognized the
6. •fWolterstorffiella Herré, 1950; 1 species. Up- Scapherpetontidae, which differs from the Dicamptodon-
per Paleocene of Germany. tídae by lacking an internal carotid foramen and by hav-
RHYACOTRITONINAE Tihen, 1958 ing the angular sepárate from the prearticular and a dif-
7. Rhyacotríton Dunn, 1920; 1 species. North- ferent pattern of palatal dentition.
western United States. J. Anderson (1968). Contení.—Five monotypic extinct genera are recog-
nized:
tSCAPHERPETONTIDAE Auffenberg
and Goin, 1959 1. tEoscapherpeíon Nessov, 1981; 1 species.
Definition.—The premaxillae are paired. The exoccip- Upper Cretaceous of Uzbekistán, U.S.S.R.
ital, prootic, and opisthotic are not fused, and the internal 2. tHorezmia Nessov, 1981; 1 species. Upper
carotid foramen is absent. The teeth are pedicellate, and Cretaceous of Uzbekistán, U.S.S.R.
the palatal denütion parallels the maxillary and premax- 3. 'fLisserpeton Estes, 1965; 1 species. Upper
illary teeth. The vertebrae are amphicoelous, and all Cretaceous and Paleocene of North America.
postsacral nerves exit intravertebrally. At least some of 4. tPiceoerpeton Meszoely, 1967; 1 species. Up-
these presumably aquatic salamanders had reduced limbs. per Paleocene tó lower Eocene of North
Fossil history.—Scapherpetonüds are known from the America.
Upper Cretaceous of southwestern Asia and from the 5. tScapherpeton Cope, 1877 (Hedronchus Cope,
1877; Hemitrypus Cope, 1877); 1 species.
Upper Cretaceous through Paleocene of North
America.

AMPHIUMIDAE Gray, 1825

Definition.—The premaxillae are fused. Septomaxil-
lae, lacrimáis, and the ypsiloid cartílage are absent, and
the pterygoids are reduced (Fig. 13-3F). The exoccipial,
prootic, and opisthotic are not fused, and the internal
carotid foramen ¡s present. The nasals are ossified from
lateral anlagen. The teeth are pedicellate, and the palatal
teeth parallel the maxillary and premaxillary teeth. The
columella is fused with the operculum. The periotic canal
is horizontal from its juncüon with a protrusion of the
periotic cistern into the fenestra ovalis. The vertebrae are
amphicoelous, and only the posterior caudal nerves exit
Figure 19-10. Amphiuma tridactylum from Texas, U.S.A. Photo through foramina in the vertebrae. The pectoral and pel-
by J. T. Collins. vic girdles are much reduced, and the limbs are vestigial.
The diploid chromosome number is 28 with a gradual
reduction from macrochromosomes to microchromo-
somes.
These large, aquatic salamanders retain some external
larval features, such as one of the three larval gilí slits
(but no external gills), and have no eyelids (Fig. 19-10).
These muscular, elongate salamanders attain total lengths
of about 1 m.
Distribution.—Living amphiumids occur on the coastal
plain of southeastern United States from Virginia to Lou-
isiana and in the Mississippi River drainage northward to
Missouri (Fig. 19-11).
Fossil history.—The family was widely distributed in
North America from the Upper Cretaceous until the up-
Figure 19-11. Distribution of living members of the family per Miocene and restricted to southeastern United States
Amphiumidae. in the Pleistocene.
 Classification
503

Figure 19-12. A. Notophthalmus

virídescens from Indiana, U.S.A.
B. Mertensíella caucásica.
C. Salamandra salamandra from
Europe. D. Tylototriton verrucosus
from Asia. Photos by J. T. Collins.

Life history.—Long strings of up to 150 eggs are laid lum. There are one or more flexures of the periotic canal
under shelter on mud near water; the eggs are guarded after its junction with a protrusion of the periotic cistern
by the female. Hatchlings are about 65 mm long and into the fenestra ovalis (horizontal canal in Notophthal-
have external gills. mus). The teeth are pedicellate, and the palatal dentítion
Remarks.—Diverse opinions on the relationships of extends posteriorly on the lateral edges of the vomers.
the amphiumids have been based on dentitíon patterns, The vertebrae are opisthocoelous, and all but the first
vertebral structure, myology, immunology, and karyol- two spinal nerves exit intravertebrally. The diploid chro-
ogy (see Estes, 1981, for summary and references). The mosome number is 22 or 24; in the latter, macrochro-
paedomorphic nature of most of the shared derived char- mosomes gradually decrease to microchromosomes.
acters, as well as the unique derived characters, make Salamandrids are highly variable in external appear-
absolute placement doubtful. ance and size. Some Salamandra and P/eurode/es attain
Contení.—Three living and three extinct species are total lengths of more than 200 mm. All salamandrids
recognized in two genera: have well-developed limbs, and many of the aquatic spe-
cies have dorsal body and caudal fins (Fig. 19-12). All
1. Amphiuma Carden, 1821 (Chrysodonía salamandrids have toxic skin secretions, and many gen-
Mitchill, 1822; Sirenoidis Fitzinger, 1843; Mu- era have bright, aposematic colors that are displayed in
raenopsis Fitzinger, 1843); 3 living and 2 ex- defense postures. The larvae have four pairs of gilí slits
tinct species. Southeastern United States. Up- and large external gills; pond larvae have balancers.
per Paleocene, Miocene, and Pleistocene of Distribution.—The Salamandridae is distributed pri-
North America. Salthe (1973). marily in Europe and Asia, where it occurs from the Brit-
2. tProampriiuma Estes, 1969; 1 species. Upper ish Isles and Scandinavia eastward to the Ural Mountains
Cretaceous of North America. in Russia and southward into the Iberian Península, Asia
Minor, and some of the Grecian islands, as well as Cor-
SALAMANDRIDAE Gray, 1825 sica and Sardinia. In central and eastern Asia, salaman-
Definition.—The premaxillae are paired in primitive drids occur from northern India, Burma, Thailand, and
genera and fused in advanced genera (Fig. 13-3E). Sep- Vietnam southeastward to Hong Kong and eastward
tomaxillae, lacrimáis, and the ypsiloid carülage are present. through China and the Japanese Archipelago. Two Eu-
The exoccipital, prootíc, and opisthotíc are fused, and ropean genera occur in extreme northwestern África, and
the internal carotid foramen is absent. A frontosquarnosal two genera are endemic to North America (Fig. 19-13).
arch is present (reduced or absent as derived states in Fossil history.—Salamandrids are especially well rep-
some genera). The columella is fused with the opercu- resented in Cenozoic deposits in Europe, where they are
EVOLUTION
504

Figure 19-13. Distribution of living

members of the family
Salamandridae.

known from the Eocene to the Pleistocene. One extinct western Spain and Portugal. Middle Mio-
genus is known from the Miocene of Asia, and the living cene of France. Busack (1976).
North American genera are known as fossils beginning 5. Cynops Tschudi, 1839; 7 species. Central
in the Oligocene. China and Japanese Archipelago. Zhao and
Life history.—Most of the genera are wholly or par- Q. Hu (1984).
tially aquatic. Courtship and reproducüve behavior is highly 6. Echinotriton Nussbaum and Brodie, 1982; 2
variable (Salthe, 1967). In Notophthalmus, there are species. Zhejiang and Hainan Island, China,
usually three distinct life forms during ontogeny—an and Ryukyu Islands. Nussbaum and Brodie
aquatic larval period of about 3 months, terrestrial sex- (1982).
ually immature stage (eft) of 2 or 3 years, and aquatic 7. Euproctus Gene, 1838 (Megapterna Savi,
adults. Tarícha and Triturus have aquatic larvae and ter- 1838; Phatnomatorhina Bibron, in Bona-
restrial adults, which return to water to breed. Cynops, parte, 1839; Pelonectes Fitzinger, 1843;
Notophthalmus, Paramesotríton, Pleurodeles, Triturus, Hemitriton Dugés, 1852; Calotriton Gray,
and Tylototriton breed in ponds; Chioglossa, Euproctus, 1858); 3 species. Pyrenees mountains of
Salamandrina, and Taricha breed in streams. Some Sal- Europe; Sardinia and Corsica. Pleistocene
amandra and Mertensiella produce living young. Individ- of Spain. Thorn (1968).
uáis in some populations oí Notophthalmus, Pleurodeles, 8. tKoa//ie//a Herré, 1950; 1 species. Upper Pa-
and Triturus are facultatively neotenic. leocene of Europe.
Remctrks.—Estes (1981) integrated data on fossil sal- 9. tMega/oíriton Zittel, 1890; 1 species. Eocene
amandrids with the phylogeny of the living genera pre- and Oligocene of Europe.
sented by D. Wake and Ózeti (1969). Brodie (1977) pro- 10. Mertensiella Wolterstorff, 1825 (Exaeretus
vided a phylogenetic assessment of antipredator behavior Waga, 1876); 2 species. Western Caucasus
in salamandrids. Mountains of Georgian S.S.R., mountains of
Contení.—The 53 living and 15 fossil species are placed eastern Turkey, and island of Karpathos,
in 15 genera; eight extinct genera contain 10 species: Greece. Lower Miocene to upper Pliocene
of Eastern Europe. Thorn (1968).
1. tArchaeotriton Meyer, 1860; 1 species. Up- 11. Neurergus Cope, 1862 (Rhithrotriton Nes-
per Oligocene and lower Miocene of terov, 1916); 4 species. Western Asia in Irán,
Czechoslovakia. Iraq, and Turkey. J. Schmidtler and F.
2. tBrac/iycormus Meyer, 1860; 1 species. Lower Schmidtíer (1975).
Miocene of Germany. 12. Notophthalmus Rafinesque, 1820 (Tristella
3. tChe/otriton Pomel, 1853 (tPo/ysemia Meyer, Gray, 1850; Diemycíy/us Hallowell, 1856);
1860; Weliarchon Meyer, 1863; tGrippie//a 3 species. Eastern North America. Miocene
Herré, 1949; tPa/aeosa/amandrina Herré, and Pleistocene of eastern United States.
1949; tTisch/erie//a Herré, 1949; tEpipo/y- Mecham (1967a, 1967b, 1968).
semia Brame, 1973); 3 species. Middle 13. tO/igosemia Navas, 1922; 1 species. Upper
Eocene to middle Miocene of Europe. Miocene of Spain.
4. Chioglossa Bocage, 1864; 1 species. North- 14. Pachytriton Boulenger, 1878 (Pingia Chang.
 Classificatíon
1936); 1 species. Mountains of southeastern gen. The columella is fused with the operculum. The 505
China. Zhao and Q. Hu (1984). periotic canal is horizontal from its junction with a pro-
15. tPa/aeopíeurode/es Herré, 1941; 1 species. trusion of the periotic cistern into the fenestra ovalis. The
Upper Oligocene of Germany. vertebrae are amphicoelous, and all but the first three
16. Paramesotriton Chang, 1935 (Mesotriton spinal nerves exit intravertebrally. The diploid number of
Bourret, 1934; Trituroides Chang, 1936); 5 chromosomes is 28.
species. North Vietnam, western and south- These moderate-sized salamanders (up to about 200
ern China, and Hong Kong. Bischoff and mm total length but up to 346 mm in Ambystoma ti-
Bohme (1980). grinum) have short, blunt heads and robust bodies and
17. Pleurodeles Michahelles, 1830 (Bradybates limbs (Fig. 19-14). Larvae have broad heads, caudal fins,
Tschudi, 1839; G/osso/iga Bonaparte, 1839); four pairs of gilí slits, and long filamentous gills; most have
2 species. Iberian Península; Morocco, Tun- balancers.
isia, and Algeria in North África. Thorn Distribución.—Ambystomatids are widespread in North
(1968). America from extreme southeastern Alaska and Labor-
18. tProcynops Young, 1965; 1 species. Mio- ador to the southern edge of the Mexican Plateau (Fig.
cene of China. 19-4).
19. Salamandra Laurenü, 1768 (tHeteroc/itotri- Fossil history.—The family is known from the lower
ton de Stefano, 1903; tCrypíobranchic/inus Oligocene through the Pleistocene of North America.
Huene, 1941; tPa/aeosa/amandra Herré, Life history.—In most Ambystoma, courtship and
1949; tVoigtieí/a Herré, 1949; Wehmielh breeding take place in ponds in the spring, but some
Herré and Lunau, 1950); 2 species. Middle species breed in the autumn and deposit eggs on land
and southern Europe, northwestern África, near water, which subsequently floods the nests. Other
and western Asia. Upper Eocene to Pleis- Ambystoma lay eggs singly or in clumps in ponds or
tocene of Europe. Thorn (1968). sluggish streams. í?hyacosiredon attaches large, unpig-
20. Sa/amandrina Fitzinger, 1826 (Seiranota mented eggs singly on stones in mountain streams. Lar-
Barnes, 1826); 1 species. Appennines vae of some species overwinter in ponds. Several species
mountains of Italy. Lower Miocene of Sar- are oblígate neotenes, whereas some others are faculta-
dinia. Thorn (1968). tívely neotenic (Table 7-4).
21. Taricha Gray, 1850 (tPa/aeotaricha van Frank, fíemarfcs.—Ambystomatids share with plethodonüds
1955); 3 species. Pacific coastal región of the most derived pattem of spinal nerves. Otherwise, they
North America. Oligocene to Pleistocene of have many character states that are primitive in the Sal-
western United States. Nussbaum and Bro- amandroidea and have no unique derived characters.
die (1981). Osteologically and reproducüvely they are generalized.
22. Trituras Rafinesque, 1815 (Tritón Laurenti, Therefore, the historical reality of the Ambystomatídae is
1768; Meínus Rafinesque, 1815; Oiacurus quesüonable.
Leuckart, 1821; Geoíriton Bonaparte, 1832; Two species are gynogenetic triploids (Table 16-4).
Lissotriton Bell, 1839; Lophinus Rafin- This family includes the famous Mexican axolotl, Am-
esque, in Gray, 1850; Ommatotriton Gray, bysíoma mexicanum, which has been used extensively
1850; Hemisalamandra Dugés, 1852; Pe- in experimental embryology and endocrinology (H. Smith
íraponia Massalongo, 1854; Pyronicia Gray, and R. B. Smith, 1971).
1858; Pelonectes Lataste, in Tourneville,
1879); 12 species. Briüsh Isles, Scandinavia,
continental Europe, Asia Minor to Caspian
Sea, eastward to Ural Mountains, U.S.S.R.
Upper Eocene to Pleistocene of Europe; up-
per Miocene of U.S.S.R. Thorn (1968).
23. Ty/ototriton Anderson, 1871; 5 species.
Northeastern India to southern China; Ryu-
kyu Islands. Eocene of Germany. Zhao and
Q. Hu (1984).

AMBYSTOMATIDAE Hallowell, 1856

Definition.—The premaxillae are paired. Septomaxil-
lae, pterygoids, and the ypsiloid cartilage are presen!, but
lacrimáis are absent (Fig. 13-3D). The exoccipital, prooüc,
and opisthotic are fused, and the internal carotid foramen
is present. The teeth are pedicellate, and the palatal teeth Figure 19-14. Ambystoma tígrínum from Lincoln County,
are transverse. The nasals are ossified from lateral anla- Missouri, U.S.A. Photo by J. T. Collins.
EVOLUTION
506

Figure 19-15. A. Desmognathus

welterí from Kentucky, U.S.A.
B. Gyrínophilus porphyríticus hora
Kentucky, U.S.A. C. Ensatina
eschscholtzi from California, U.S.A.
D. Pseudoeurycea cephalíca from
Morelos, México. A-C by J. T.
Collins; D by W. E. Duellman.

Content.—Two living genera contain 30 species; 5 other 4). The exoccipital, prooüc, and opisthoüc are fused, and
species are known only as fossils, 1 in an extinct genus: the internal carotid foramen is absent. The teeth are ped-
icellate, and the palatal teeth extend posteriorly along the
1. Ambystoma Tschudi, 1838 (Gyrinus Shaw and medial edges of the vomers. The nasals are ossifed from
Nodder, 1789; Axolotus Jaroki, 1822; Phil- lateral anlagen. Lacrimáis, pterygoids, lungs, and the yp-
hydrus Brookes, 1828; Siredon Wagler, 1830; siloid cartilage are absent, but pterygoids are present in
Axolotl Bonaparte, 1831; Sirenodon Wieg- larvae. The operculum is absent, and it is replaced func-
mann, 1832; Síegoporus Wiegmann, 1832; tionally by the footplate of the columella. There are one
Xiphonura Tschudi, 1838; Sa/amandroidis or more flexures of the periotic canal from its junction
Fitzinger, 1843; Axolotes Owen, 1844; Am- with a protrusion of the periotic cistern into the fenestra
b/ysíoma Agassiz, 1844; Heterotriton Gray, ovalis (canal horizontal in Batrachoseps and Thoríus).
1845; Limnarches Gistel, 1848; Xiphoctonus The vertebrae are opisthocoelous, and all but the first
Gistel, 1848; Plagiodon Duméril, Bibron, and three spinal nerves exit intravertebrally. The diploid num-
Duméril, 1854; Desmiostoma Sager, 1858; ber of chromosomes is 26 or 28.
Camarataxís Cope, 1859; Pectoglossa Mivart, Plethodontids are highly variable in size and shape.
1867; Linguaelapsus Cope, 1887; tP/ioam- Some species of Thoríus have total lengths of no more
bystoma Adams, 1929; Bathysiredon Dunn, than 27 mm, whereas the largest species are Oedipina
1939; tLanebatrachus Taylor, 1941; tOga/- collaris (253 mm) and Pseudoeurycea bella (325 mm).
lalabatrachus Taylor, 1941); 26 species. North Some plethodontíds are slender and elongate (e.g., Ba-
America from southern Canadá to central trachoseps, Lineatriton, and Oedipina), whereas others
México. Lower Oligocene through the Pleis- (e.g., desmognathines) are robust (Fig. 19-15). Some
tocene of North America. Tihen (1969). Bolitoglossa and Chiropterotriton have webbed feet, and
2. tAmphiíriton Rogers, 1976; 1 species. Upper Aneides, BoÜtoglossa, and Pseudoeurycea have prehen-
Pliocene of Texas, U.S.A. sile tails. Males of most genera have protuberances (cirri)
3. Rhyacosiredon Dunn, 1928; 4 species. Moun- on the upper lip associated with the nasolabial grooves
tains of central México. Tihen (1958). and also have mental glands. Two genera (Haideotriton
and Typh/omo/ge) are oblígate neotenes.
PLETHODONTIDAE Gray, 1850 Distribution.—Plethodontids occur in eastern and
Definition.—The premaxillae usually are paired (fused western North America from Nova Scoüa and extreme
in many genera). Maxillae and premaxillae are present southeastern Alaska southward, with some species in the
(secondarily reduced or absent in some genera; Fig. 13- central región (absent from the Great Plains, most of the
 Classificatíon
Rocky Mountains, and the Great Basin). A major center ton, Stereochilus, Typh/omo/ge, and Typhlotriton); (2) 507
of differentiation is in México and Central America, where Plethodontini characterized by lacking aquatic larvae and
the family occurs in all but the xeric regions. Two genera having large, ossified second basibranchial, and contain-
enter South America, where the family extends from Co- ing three genera (Aneides, Ensatina, andP/etnodonj; and
lombia to eastern Brazil and central Bolivia (Fig. 19-16). (3) Bolitoglossini characterized by lacking aquatic larvae
Two species of Hydromantes occur in southern Europe and second basibranchials, and containing all of the other
and on Sardinia; otherwise the genus is restricted to cen- plethodontine genera.
tral California in North America. Contení.—Two subfamilies contain 27 genera and 220
Fossil histoty.—Six Recent genera are known from species:
the lower Miocene to the Pleistocene of North America.
Life history.—Most desmognathines and the members DESMOGNATHINAE Cope, 1859
of the tribe Hemidactyliini of the plethodontines have 1. Desmognathus Baird, 1850; 11 species.
aquatic eggs and larvae, which have branched gills and Southeastern Canadá and eastern United
no balancers. Other plethodontids have direct develop- States west to Oklahoma and Texas. Pleis-
ment of terrestrial eggs. Although the major evolutionary tocene of Virginia and Texas. D. Wake
trend in life history of plethodontids has been from aquatic (1966), Tilley et al. (1978), Tilley (1981).
eggs and larvae to direct development of terrestrial eggs, 2. Leurognathus Moore, 1899; 1 species.
some subterranean salamanders have remained in a lar- Southern Appalachian Mountains, U.S.A.
val state. This trend is seen in Eurycea and Gyrinopni/us, Martof (1963).
in which some species metamorphose and others do not; 3. Phaeognathus Highton, 1961; 1 species.
extreme cases of paedomorphosis are exhibited by the Southern edge of Red Hills región, Ala-
oblígate neotenes Haideotriton and Typh/omo/ge. bama, U.S.A. Branden (1966b).
Remarte.—The evolutionary relationships among
plethodontids were reviewed by Larson (1984). The two PLETHODONTINAE Gray, 1850
subfamilies were defined by D. Wake (1966), as follows: 4. Aneides Baird, 1849 (Autodox Boulenger,
Desmognathinae—(1) four larval gilí slits; (2) unique 1887); 5 species. Pacific coast of North
mouth-opening mechanism by means of which the man- America; Sacramento Mountains of New
dibles are held rigid and the skull raised; (3) well-devel- México; Appalachian Mountains and asso-
oped hypapophysial keels on anterior trunk vertebrae. ciated piedmont of eastern U.S.A. Lower
Plethodontinae—(1) three larval or embryonic gilí slits; Miocene of Montana, U.S.A. D. Wake (1974).
(2) normal mouth opening mechanism by means of which 5. Batracnoseps Bonaparte, 1841 (Plethopsis
the skull remains rigid and the mandibles are lowered; Bishop, 1937); 8 species. Western North
(3) no well-developed hypapophysial keels on vertebrae. America. Lower Pliocene of California, U.S.A.
D. Wake (1966) recognized three tribes in the Pletho- Yanev (1980).
dontinae: (1) Hemidactyliini characterized by having 6. Bolitoglossa Duméril, Bibron, and Duméril,
aquatic larvae and containing eight genera (Eurycea, 1854 (Oedipus Tschudi, 1838; Eladinea Mi-
Gyrinopni/us, Haideotriton, Hemidactylium, Pseudotri- randa-Ribeiro, 1937; Magnadigita Taylor,

Figure 19-16. Distribution of living

members of the family
Plethodontidae.
EVOLUTION
508 1944; Palmatotriton Smith, 1945); 67 spe- North America; Rocky Mountains in New
cies. Northeastern México to eastern Brazil México, U.S.A. Highton and Larson (1979).
and central Bolivia. D. Wake and J. F. Lynch 22. Pseudoeurycea Taylor, 1944; 25 species.
(1976), D. Wake and P. Elias (1983). México and Guatemala. D. Wake and P. Elias
7. Bradyíriton Wake and Elias, 1983; 1 species. (1983).
Sierra de los Cuchumatanes, Guatemala. D. 23. Pseudotriton Tschudi, 1838 (Mycetog/ossus
Wake and P. Elias (1983). Bonaparte, 1839; Batrachopsis Fitzinger,
8. Chiropterotríton Taylor, 1944; 9 species. 1843; Pe/odytes Gistel, 1848); 2 species.
Eastern México. D. Wake and P. Elias (1983). Appalachian uplift of eastern United States.
9. Dendrotriton Wake and Elias, 1983; 5 spe- Martof (1975).
cies. Southwestern Chiapas, México, and 24. Stereochilus Cope, 1869; 1 species. Atlantic
western Guatemala. D. Wake and P. Elias Coastal Plain from Virginia to Georgia, U.S.A.
(1983). Pleistocene of Maryland and Georgia, U.S.A.
10. Ensatma Gray, 1850 (Hereda Girará, 1856; G. Rabb (1966).
Urotropis Jiménez de la Espada, 1870); 25. Thorius Cope, 1869; 9 species. Mountains of
1 species. Pacific coast and Sierra Nevada southern México. D. Wake and P. Elias
in western North America. Stebbins (1949b). (1983).
11. Eurycea Rafinesque, 1822 (Spelerpes Rafin- 26. Typhlomolge Stejneger, 1896; 2 species.
esque, 1832; Cy/indrosoma Tschudi, 1838; Subterranean waters of central Texas, U.S.A.
Saurocercus Fitzinger, 1843; Manculus Cope, Potter and Sweet (1981).
1869); 11 species. Eastern North America 27. Typhlotriton Stejneger, 1893; 1 species. Ozark
westward to Ozark uplift and to central Texas. uplift of south-central United States. Bran-
D. Wake (1966). don (1970b).
12. Gyrínophilus Cope, 1869; 2 species. Appa-
lachian uplift of eastern North America. Order GYMNOPHIONA Rafinesque, 1814
Pleistocene of eastern United States. Bran- Definition.—Caecilians are elongate, limbless amphib-
don (1967a). ians that are highly specialized for burrowing. The body
13. Haideotríton Can, 1939; 1 species. Subter- is greatly elongate and segmented by annular grooves
ranean waters in southern Georgia and the (containing scales in some species). The tail, if present,
Florida panhandle, U.S.A. Brandon (1967b). is short and pointed. The eyes are small and covered
14. Hemiddcry/ium Tschudi, 1838 (Coíoboíes with skin or bone. The vertebrae are amphicoelous, and
Gistel, 1848; Desmodacty/us Duméril, Bi- the ribs are bicapitate. Sternal elements, girdles, and limbs
bron, and Duméril, 1854; Dermodacíyíus are absent. The skull is compact with fusión of some
David, 1875); 1 species. Eastern North elements (e.g., maxilla and palatine into maxillopalatine,
America. Neill (1963). and the otic and occipital elements, and the parasphe-
15. Hydromctntes Gistel, 1848 (Hydromctntoides noid into the básale). The columella (stapes) ¡s massive
Lanza and Vanni, 1981); 5 species. Moun- or absent. The teeth generally are curved and are present
tains of central and northern California, on the premaxillae, maxillopalaünes, vomers, dentarles,
U.S.A; northem Italy to southwestern France; and usually on the splenials. The left lung usually is ru-
Sardinia. D. Wake et al. (1978). dimentary. A protrusible, sensory tentacle is present be-
16. Lineatriton Tanner, 1950; 1 species. Eastern tween the eye and the nostril. Males have a single, me-
México. D. Wake and P. Elias (1983). dian, protrusible copulatory organ (phallodeum). Aquatic
17. Nototñton Wake and Elias, 1983; 6 species. larvae (if present) have gilí slits but no external gills.
Guatemala to Costa Rica. D. Wake and P. Distríbution.—Caecilians are pantropical. Three fam-
Elias (1983). ilies occur in southeastern Asia (one including the Ori-
18. Nyctanolis Elias and Wake, 1983; 1 species. ental part of the Indo-Australian Archipelago eastward to
Mountains of northern Guatemala and ad- Borneo and the Philippines). Two families (one endemic)
jacent México. P. Elias and D. Wake (1983). are in tropical África, and three families (two endemic)
19. Oedipina Keferstein, 1868 (Ophiobatrachus occur in the American tropics. Three genera are endemic
Gray, 1868; Haptoglossa Cope, 1893; Oed- to the Seychelles islands in the Indian Ocean, but cae-
opino/a Hilton, 1946); 16 species. Chiapas, cilians do not occur on other islands in the Indian Ocean.
México, to northwestern Ecuador. Brame including Madagascar.
(1968). Fossil history.—The single recognized caecilian fossil
20. Parvimolge Taylor, 1944; 1 species. Eastern is from the Paleocene of Brazil.
México. D. Wake and P. Elias (1983). Life history.—Presumably all caecilians have internal
21. Plethodon Tschudi, 1838 (Sauropsis Fitzin- fertílization. Primitive caecilians are oviparous and have
ger, 1843); 26 species. Eastern and Western aquatic larvae. Some advanced caecilians are oviparous;
 Classification
509

Figure 19-17. Distribution of living

members of the family
Rhinatrematidae in South America
and of the family Ichthyophiidae in
Asia.

their eggs undergo direct development into terrestrial and temporal fossae are present. The sides of the para-
young. Most advanced caecilians are viviparous. The foe- sphenoid are parallel, and the vomers are separated by
tuses have specialized teeth (shed at birth) with which the cultiform process of the parasphenoid. The columella
they scrape the epithelial lining of the oviduct and obtain is pierced by the stapedial artery and is movably attached
nutriente secreted by the oviducal cells (M. Wake, 1977a). to the quadrate, which articulates with the maxillopala-
Remar/es.—Caecilians are the least-known group of tine. The retroarticular process of the pseudoangular is
living amphibians. Although their morphology has long short and horizontal. Dorsolateral processes are present
been of interest to anatomists (e.g., Wiedersheim, 1879; on the básale.
P. Sarasin and F. Sarasin, 1887-1890), only recently Rhinatrematids are small caecilians (largest is Epicrion-
have comparative studies been undertaken. E. Taylor's ops petersi with a total length of 328 mm) and have a
(1968) monograph of caecilians was supplemented by tail and a terminal mouth. The tentacular opening is ad-
his comparative studies of skulls (1969b), scales (1972), jacent to the anterior edge of the eye. Primary and sec-
vertebrae (1977a), and mandibles (1977b). Nussbaum ondary annuli are orthoplicate, present throughout the
and Naylor (1982) reported on the trunk musculature. length of the body, and bear scales. Rhinatrema is slen-
The urogenital system has been studied by M. Wake der and has yellow lateral stripes, like some species of
(1972 and papers cited therein). The teeth have been Epicrionops, but some of the latter are unicolor and some
studied by M. Wake (1980d and papers cited therein), others are thick-bodied. Larvae have obvious lateral-line
and vertebrae have been investigated by M. Wake (1980c). systems and a single gilí slit.
M. Wake and Hanken (1982) provided data on the on- Distribution.—Rhinatrematids are restricted to South
togenetic development of the skull and summarized pre- America where they occur in Caribbean, Amazonian, and
vious work on that subject. Nussbaum (1977,1979a) has Pacific drainages from Venezuela to Perú, and in the
made the only attempts at phylogenetic reconstructions Guianan región (Fig. 19-17).
of caecilians. Fossil history.—None.
The ordinal ñame Apoda sometimes used for caecili- Life history.—Larvae are known for some species of
ans was applied first to a group of eel-like fishes and is Epicrionops, and Rhinatrema is presumed to have a lar-
not available for caecilians. val stage. Larvae of E. petersi have been found in mud
Contení.—Six families are recognized; these contain at the edge of a stream.
34 living genera and 162 species and 1 extinct genus and Remarks—Nussbaum (1977) showed that rhinatre-
species. matids possess a suite of primitive characters that distin-
guish them from the more advanced ichthyophiids. Fur-
RHINATREMATIDAE Nussbaum, 1977 thermore, rhinatrematids have a uniquely derived feature—
Definition.—The skulls of the most primitive family of paired dorsolateral processes of the básale that fit into
caecilians are kinetic and zygokrotaphic (Fig. 13-10). The notches in the posterior ends of the squamosals. These
premaxillae are sepárate from the nasals; septomaxillae provide support to the cheek región and are important
and postfrontals are present, but discrete prefrontals are structural supports in an otherwise relatively weak, zygo-
absent. The squamosals do not articúlate with the frontal, krotaphic skull.
EVOLUTION
510 Contení.—Two genera with nine species are recog- gilí slits, and shallow caudal fins. The three pairs of em-
nized: bryonic gills apparently are absorbed at hatching.
Distribution.—The family is widespread in southeast-
1. Epicrionops Boulenger, 1883; 8 species. ern Asia, including the Indian subconünent, Sri Lanka,
Northwestern South America from Venezuela Sumatra, Borneo, and the Philippines (Fig. 19-17).
to Perú. E. Taylor (1968). Fossil history.—None.
2. Rhinatrema Duméril and Bibron, 1841; 1 spe- Life history.—Eggs are deposited in mud near water;
cies. Guianan región of northeastern South as many as 54 eggs are in a single clutch of ¡chthyophis
America. Nussbaum and Hoogmoed (1979). glutinosus, females of which guard the eggs. Free-swim-
ming larvae live in ponds and streams.
ICHTHYOPHIIDAE Taylor, 1968 Remarks.—Nussbaum (1979a) included the Uraeo-
Deflnition.—These Oíd World caecilians have a com- typhlidae as a subfamily of the Ichthyophiidae. Although
binatíon of primitive and derived characters that are inter- the two families have many characters in common, the
medíate between those of rhinatrematids and other cae- uraeotyphlids are cladistically closer to the higher families
cilians. The premaxillae are sepárate from the nasals; of caecilians than to the ichthyophiids and are recognized
septomaxillae and prefrontals are present, and discrete herein as a sepárate family.
postfrontals usually are present (Fig. 13-11). The squa- Contení.—Two genera with 35 species are recognized:
mosals articúlate with the frontal, and temporal fossae
are absent. The pterygoids are not in contact with the 1. Caudacaecilia Taylor, 1968; 5 species. Malaya,
parasphenoid portion of the básale. The sides of the Sumatra, Borneo, and the Philippines. E.
parasphenoid are not parallel, and the vomers are in Taylor (1968).
contact medially. The columella is pierced by the stape- 2. ¡chthyophis Fitzinger, 1826 (Epícrium Wagler,
dial artery. There is no bridge between the quadrate and 1828); 30 species. India, Sri Lanka, south-
the maxillopalatine. The retroarticular process of the eastern Asia, southern Philippines, and west-
pseudoangular is long and curved. ern part of Indonesia. E. Taylor (1968).
These moderate-sized caecilians (total length to about
500 mm) have a tail and a subterminal mouth. The ten- URAEOTYPHLIDAE Nussbaum, 1979
tacular opening is midway between the eye and the nos- Definition.—This family of caecilians shares many
tril or closer to the eye. Primary and secondary annuli characters with the ichthyophiids, but uraeotyphlids are
(2-4 secondaries per primary) are present throughout the cladistically more closely related to the higher caecilian
length of the body, bear scales, and are orthoplicate pos- families than to the Ichthyophiidae. The premaxillae are
teriorly. Some ichthyophiids are unicolor gray or black; sepárate from the nasals; septomaxillae, prefrontals, and
others have bold palé stripes laterally (Fig. 19-18). Lar- postfrontals are present. The squamosals articúlate with
vae have well-developed lateral-line systems, one or two the frontal, and small temporal fossae are present. The

Figure 19-18. /chthyophis

kohtaoensis from Thailand. Photo by
M. H. Wake.
 Classificatíon
511

Figure 19-19. Distribution of living

members of the family
Uraeotyphlidae ¡n India and of the
family Scolecomorphidae in África.

pterygoids are in weak contact with the parasphenoid

portíon of the básale. The sides of the parasphenoid are
not parallel, and the vomers are in contact medially. The
columella is unperforated. There is no bridge between
the quadrate and the maxillopalatine. The retroarticular
process of the pseudoangular is long and curved.
These small caecilians (total length to about 300 mm)
have a tail and a recessed mouth. The tentacular opening
is below the nostril. Primary and secondary annuli are
present throughout the length of the body; they bear
scales, and they are not complete anteriorly. These cy-
lindrical caecilians are dull gray to brown. The larvae are
unknown.
Distribution.—This family is known only from south-
ern peninsular India (Fig. 19-19). Figure 19-20. Scolecomorphus uluguruensis from África. Photo
Fossil history.—None. by B. Fritzsch.
Life history.—Presumably these caecilians are ovipa-
rous, possibly with direct development.
Remarks.—Nussbaum (1979a) showed that these septomaxillae and prefrontals are present, but postfron-
caecilians are cladistícally closer to higher caecilians than tals, pterygoids, and colurnellae are absent. The squa-
to ichthyophiiids, but he regarded tham as a subfamily mosals do not articúlate with the frontal. Temporal fossae
of the Ichthyophiidae. The phylogeneüc position of these are absent in West African species and present in East
caecilians is better shown by treating them as a sepárate African species. The sides of the parasphenoid are not
family. parallel, and the vomers are in contact medially. There
Contení.—The single genus contains four species: is no bridge between the quadrate and the maxillopala-
tine. The retroarticular process of the pseudoangular is
1. Uraeotyphlus Peters, 1879; 4 species. South- long and curved. The eye is covered with bone and pro-
ern India. Nussbaum (1979a). truded on the tentacle.
These are moderately large caecilians with a recessed
SCOLECOMORPHIDAE Taylor, 1969 mouth and no tail; Scolecomorphus convexas attains a
Deflnition.—These African caecilians have a suite of total length of 448 mm. Secondary annuli and scales are
unique character states that set them apart from all other absent. The dorsum is black or brown; in some species
caecilians. The premaxillae are sepárate from the nasals; the venter is palé (Fig. 19-20).
EVOLUTION
512 Distribution.—The family has a discontinuóos range the quadrate and the maxillopalatine. The retroarticular
in tropical, sub-Saharan África (Fig. 19-19); two species process of the pseudoangular is long and cutved.
are known from Cameroon and three from Tanzania and Caeciliids have a recessed mouth and no tail. The ten-
Malawi. tacular opening is anterior to the eye. Secondary annuli
Fossil history.—None. are absent anteriorly or throughout the length of the body;
Life history.—Embryos with branched gills are like those scales are present or absent. Although most caeciliids are
of species of Dermophis that are viviparous. dull gray or black, some are striped; Boulengerula bou-
Remarks.—The skull of scolecomorphids seems to be lengerí and Microcaeciha albiceps have pink heads, and
adapted for burrowing in a different way than those of Schistometopum thomense is bright yellow (Fig. 19-21).
caeciliids. Although the skull of scolecomorphids is zygo- Many species are small; Idiocranium russeli and Gran-
krotaphic with no fusión or loss of roofing bones, it seems disonia brevis attain lengths barely exceeding 100 mm,
to be akinetic. whereas some species grow to lengths of more than 1
Contení.—One genus contains seven species: m. The largest is Caecilia thompsoni with a total length
of 1520 mm.
1. Scolecomorphus Boulenger, 1883 (Bdellophis Distribution.—The family is distributed throughout the
Boulenger, 1895); 7 species. Tropical sub- tropical regions of South and Central America (13 gen-
Saharan África. Nussbaum (1981). era), sub-Saharan África (6 genera), and the Indian sub-
continent (2 genera); 3 genera are endemic to the Sey-
CAECILIIDAE Gray, 1825 chelles islands in the Indian Ocean (Fig. 19-22).
Definition.—These terrestrial caecilians have many Fossil history.—The single known fossil caecilian,
derived character states shared with other families. The Apodops prícei from the Paleocene of Brazil, tentatively
premaxillae are fused with the nasals. Septomaxillae and is referred to this family. Estes and M. Wake (1972) in-
prefrontals are absent, and postfrontals usually are ab- dicated that the fossil vertebra is similar to those of the
sent. The squamosals articúlate with the frontal, and tem- Recent African genus Geotrypetes.
poral fossae are absent (except Geotrypetes). The pter- Life history.—Some species lay eggs that undergo di-
ygoids are fused with the maxillopalatines. The sides of rect development; others are viviparous. Embryonic gills
the parasphenoid are not parallel, and the vomers usually are triradiate; these and the lateral-line organs (present
are in contact medially (separated by the cultriform process in some species) are resorbed before birth or hatching.
of the parasphenoid in some genera). The columella is The reproductive mode of too few species is known to
perforated or not by the stapedial artery and is firrnly draw any conclusions, but most of the New World species
arüculated with the quadrate. There is no bridge between for which reproductive data are available are viviparous,
and the Indian and Seychellean species are oviparous.
Both oviparity and viviparity are known in African cae-
ciliids.
Remarks.—All of the highly specialized burrowing
caecilians with stegokrotaphic skulls are grouped in this
family. Although most of the known genera and species
were reviewed by E. Taylor (1968), the intrafamilial re-
lationships remain obscure. Two subfamilies were pro-
posed by Taylor (1969a) and their contents modified by
M. Wake and Campbell (1983). Laurent (1984) sug-
gested that the Caeciliidae should contain only Caecilia
and Oscaecilia and that the other genera should be placed
is the Dermophiidae with two subfamilies—the Dermo-
phiinae in which splenial teeth are absent (except in
Gymnopis) and containing all of the New World genera,
and the Herpelinae in which splenial teeth are present
(except in Boulengerula) and containing all of the Oíd
World genera. However, the character of the fusión of
the postfrontal used by Laurent to define the Caeciliidae
is not consistent in the genus Caecilia, and the characters
used to define the Herpelinae and Dermophiinae are not
consistent within those subfamilies (as defined by Lau-
rent). Herein two subfamilies are recognized: Dermo-
phiinae with maxillary and premaxillary teeth not en-
Figure 19-21. A. Oscaecilia ochrocephala from Panamá.
B. Dermophis mexicanas from Chiapas. México. Photos by M. H. larged, and Caeciliinae with maxillary and premaxillary
Wake. teeth enlarged.
 Classification
513

Figure 19-22. Distribution of living

members of the family Caeciliidae.

Contení.—Twenty-four living genera and one extínct 12. Gegeneophis Peters, 1879 (Gegenes Günther,
genus contain 88 living and 1 extínct species are grouped 1875); 3 species. India. E. Taylor (1968).
into two subfamilies: 13. Geotrypetes Peters, 1879; 4 species. Tropical
West África and western Ethiopia. E. Taylor
CAECILIINAE Gray, 1825 (1968).
1. Caedlia Linnaeus, 1758 (Amphiumophis 14. Grandisonia Taylor, 1968; 5 species. Sey-
Werner, 1901); 31 species. Northern South chelles islands. E. Taylor (1968).
America and eastern Panamá. E. Taylor 15. Gymnopis Peters, 1874 (Cryptosophus Bou-
(1968). lenger, 1883); 1 species. Honduras to Pan-
2. Microcaecilia Taylor, 1968; 5 species. North- amá. J. Savage and M. Wake (1972).
ern South America. Nussbaum and Hoog- 16. Herpe/e Peters, 1879; 2 species. Tropical West
moed (1979). África. E. Taylor (1968).
3. Minascaecilia Wake and Campbell, 1983; 1 17. Hypogeophis Peters, 1879; 1 species. Sey-
species. Guatemala. M. Wake and Campbell chelles islands. E. Taylor (1968).
(1983). 18. Idiocranium Parker, 1936; 1 species. Nigeria.
4. Oscaecilia Taylor, 1968; 7 species. Panamá E. Taylor (1968).
and northern South America. E. Taylor 19. Indotyphlus Taylor, 1960; 1 species. India. E.
(1968). Taylor (1968).
5. Pawicaecilia Taylor, 1968; 2 species. North- 20. Lutkenotyphlus Taylor, 1968; 1 species.
ern Colombia. E. Taylor (1968). Southeastem Brazil. E. Taylor (1968).
DERMOPHIINAE Taylor, 1969. 21. Mimosiphonops Taylor, 1968; 1 species.
6. Afrocaecilia Taylor, 1968; 3 species. Tanza- Southeastem Brazil. E. Taylor (1968).
nia and Kenya. E. Taylor (1968). 22. Pras/inia Boulenger, 1909; 1 species. Sey-
7. tApodops Estes and Wake, 1972; 1 species. chelles islands. E. Taylor (1968).
Upper Paleocene of southeastem Braal. Estes 23. Pseudosiphonops Taylor, 1968; 1 species.
and M. Wake (1972). Brazil. E. Taylor (1968).
8. Boulengerula Tornier, 1897; 1 species. Usa- 24. Schistometopum Parker, 1941; 5 species.
mabara and Magrotto mountains, Tanzania. Kenya, Tanzania, and islands in the Gulf of
E. Taylor (1968). Guinea, West África. E. Taylor (1968).
9. Brazilotyphlus Taylor, 1968; 1 species. Am- 25. Siphonops Wagler, 1830; 6 species. Tropical
azon Basin, Brazil. E. Taylor (1968). South America east of the Andes. E. Taylor
10. Copeotyphlmus Taylor, 1968; 1 species. (1968).
?Northern Honduras. Nussbaum (1979c).
11. Dermophis Peters, 1879; 3 species. Southern TYPHLONECTIDAE Taylor, 1968
México to northwestern Colombia. J. Sav- Definition.—These aquatic caecilians have a suite of
age and M. Wake (1972). derived characters. The premaxillae are fused with the
EVOLUTION
514 are not parallel, and the vomers are in contact medially.
The columella is unperforated and is firmly attached to
the quadrate. There is no bridge between the quadrate
and the maxillopalatine. The retroarticular process of the
pseudoangular is long and curved.
Typhlonectids are completely aquatic (Fig. 19-23); the
posterior part of the body is laterally compressed. There
is no tail, and the mouth is recessed. Secondary annuli
and scales are absent. The largest species, Typhlonectes
eiselti, attains a total length of 725 mm. The dorsal color
is gray to olive brown or bluish black, and the venter
usually is a paler color. The choanae have well-devel-
oped valves, and the tongue has large narial plugs. The
Figure 19-23. Typhlonectes compressicauda from Leticia, tentacle is small and usually protrudes just behind the
Colombia. Photo by M. H. Wake. nostrils. Males have modified anal regions that seem to
serve for adhering the vent to the cloaca of the female
during aquatic copulation.
Distribution.—The family has a discontinuous distri-
bution in South America with the majority of the species
in the northwestern part of the continent—Amazon, Or-
inoco, and Magdalena river drainages, but several species
occur in the Río La Plata drainage in Argentina and Brazil
(Fig. 19-24).
Fossil history.—None.
Life history.—Embryos of these viviparous caecilians
have one pair of expanded, sheetlike externa! gills. These
are resorbed, and the gilí slits cióse before birth.
Remarks.—Nussbaum (1977) emphasized that the
skulls of typhlonectids are like those of caeciliids special-
ized for burrowing; thus, he suggested that the aquatic
typhlonectids evolved from a fossorial ancestor.
Content.—Four genera contain 19 species;

1. Chthonerpeton Peters, 1879; 6 species.

Southern Brazil and northern Argentina. E.
Taylor (1968).
2. Nectocaecilia Taylor, 1968; 5 species. Amazon
Basin and Caribbean drainages in South
America; ?Buenos Aires. E. Taylor (1968).
3. Potomotyphlus Taylor, 1968; 2 species. Am-
azon and Orinoco Basins, South America. E.
Taylor (1968).
4. Typhlonectes Peters, 1879; 6 species. North-
ern South America. E. Taylor (1968).

Superorder SALIENTIA Laurenti, 1768

Deflnition.—Primitive salientians have a short tail; in
anurans the caudal vertebrae are fused into a postsacral
Figure 19-24. Distribution of living members of the family
Typhlonectidae. rod, the coccyx (or urostyle). The vertebral column con-
tains no more than 14 presacral vertebrae. The ilia and
proximal tarsal elements are elongated. The parasphe-
noid usually bears lateral alae posteriorly, and the pter-
nasals; septomaxillae, prefrontals, and postfrontals are goid usually is triradiate. Teeth are absent on the dentary
absent. The squamosals articúlate with the frontal; tem- (except in one Recent species). Lacrimal, postorbital, ju-
poral fossae are present. The pterygoids usually are fused gal, postfrontal, postparietal, tabular, supratemporal, su-
with the maxillopalatínes. The sides of the parasphenoid praoccipital, basioccipital, and ectopterygoid bones are
 Classificaüon
absent. Ribs are present in some taxa. The aquatic larvae America and Eurasia. Four families occur in Australia, 515
(when present) lack true teeth, and most have internal and four are on Madagascar; one family is endemic to
gills with branchial baskets. the Seychelles islands in the Indian Ocean.
Contení.—The superorder contains the Triassic frog- Fossil history.—Anurans are rather poorly repre-
like Triadobatrachus and the anurans. sented in the fossil record beginning in the Jurassic of
Europe, North America, and South America and extend-
Ordcr tPROANURA Romer, 1945 ing through the Pleistocene. Six named fossil genera of
The oldest known salientian has many froglike features anurans are not assignable to recognized families:
(see account of tProtobatrachidae for characters and dis-
1. tComobarrac/ius Hecht and Estes, 1960; 1
cussion).
species. Late Jurassic of North America.
2. tEobaírachus Moodie, 1912; 1 species. Late
tPROTOBATRACHIDAE Piveteau, 1937
Jurassic of North America.
Deflnition.—A single fossil from the Triassic has a total
3. tEorubeta Hecht, 1960; 1 species. Eocene of
length of about 100 mm, a broad head with large, paired
North America.
(?) frontoparietals, triradiate pterygoids, and palatines
4. tMontsechobatrachus Fejérváry, 1923; 1 spe-
present only laterally (?). There are 14 presacral verte-
cies. Late Jurassic or Early Cretaceous of Spain.
brae lacking transverse processes and bearing bicapitate
5. tTheaíonius Fox, 1976; 1 species. Late Cre-
ribs that presumably articúlate in a manner similar to that
taceous of North America.
of salamanders and caecilians; six postsacral (caudal) ver-
6. tTregobaírac/ius Holman, 1975; 1 species.
tebrae are present. The ilial shaft is elongate and has a
Lower Pliocene of North America.
dorsal prominence. The proximal tarsal elements, the übiale
and fibulare (= astragalus and calcaneum) are elongate Additionally, nine nominal genera are of unknown sta-
but not fused. tus; these are tAsphaerion Meyer, 1847; tBaryboas Gis-
Fossil history.—This family is represented by a single tel, 1848; tBatracfiu/ina Kuhn, 1962; tBarrachus Pomel,
nodule with dorsal and ventral impressions of the skel- 1853; tBu/onopsis Kuhn, 1941; tOpisf/iocoe/ei/us Kuhn,
eton from the Lower Triassic of Madagascar. 1941; tOpisthocoe/orum Kuhn, 1941; tProfophrynus
Remarks.—According to Estes and Reig (1973), who Pomel, 1853; and tfíanauus Portis, 1885.
summarized previous work on this fossil, the specimen Life history.—Anurans have a diversity of reproduc-
probably represents a young individual of an aquatic an- tive modes. Fertilization is external, except in Ascaphus,
imal that may be the sister group of anurans. Mertensophryne micranotis, and some species of Nec-
Contení.—There is a single monotypic genus: tophrynoides and Eleutherodactylus. The generalized (and
presumably primitive) mode of life history involves aquatic
1. tTriadobatrachus Kuhn, 1962 (tProtobatra- eggs and larvae. Specialized modes include deposition of
chus Piveteau, 1937); 1 species. Lower Trias- eggs out of water but aquatic tadpoles, terrestrial eggs
sic of Madagascar. undergoing direct development, ovoviviparity, and vivi-
parity. Many kinds of anurans exhibit parental care by
Order ANURA Rafinesque, 1815 guarding or transporting eggs or tadpoles (for details, see
Deflnition.—The frogs and toads are tailless amphib- Chapter 2).
ians with elongate hindlimbs; the foot is lengthened by Remarks.—The higher taxonomy of anurans is not
the elongated proximal tarsal elements, the übiale and well established. Present knowledge of many characters
fibulare ( = astragalus and calcaneum), which are fused and the direction of their evolutionary change does not
at least proximally and distally. The vertebral column permit their utilization in the reconstruction of a phylog-
consists of 5-9 (modally 8) presacral vertebrae. All ver- eny (Chapter 17) or the concomitant construction of a
tebrae bear transverse processes, except the first (atlas) meaningful classification of anurans. Recent attempts at
unless it is fused with Presacral II. Ribs are freely asso- a classification of anurans by Duellman (1975), Laurent
ciated with, or fused to, the second, third, and fourth (1979), and Dubois (1983) have maintained paraphyletic
(also fifth and sixth in some) presacral vertebrae in some groups. P. Starrett's (1973) classification based on larval
primitíve families. The postsacral vertebrae are fused into characters was disputed by Sokol (1975) in his re-eval-
a rodlike coccyx. The otic-occipital región is composed uation of larval characters. Moreover, the placement of
of prootics and exoccipitals (fused or unfused). some genera and subfamilies has shifted from one family
Distríbution.—Anurans are cosmopolitan except for to another. For example, are the Madagascaran mantel-
high latitudes in the Arctic, Antárctica, some oceanic is- lines ranids or rhacophorids? Or, are the Madagascaran
lands, and some extremely xeric deserts. The greatest scaphiophrynines ranids or microhylids? Some workers
diversity of anurans is in the tropics. Nine families occur recognize the Myobatrachidae; others include those Aus-
in South America, eight in África, and seven in tropical tralo-Papuan frogs in the Leptodactylidae. Are the South
Asia, whereas only six occur in each of températe North African frogs of the genus Heleophryne leptodactylids,
EVOLUTION
516 myobatrachids, or neither? Are the relationships of the archaic and transitional families. Based on apparent de-
Sooglossidae with the megophryine pelobatids, myoba- velopmental differences of the frontoparietals, Ro£ek
trachids, or ranids? Probably when a well-corroborated (1981) proposed the order Archaeosalientia for Pe/o-
cladogram has been constructed these questions will be tates, pipids, palaeobatrachids, and rhinophrynids; the
seen to have been the result of confusión between sim- other anurans and Tríadobatrachus were placed in the
ilarity based on retained primitive features and similarity order Neosalientia.
based on shared-derived features. The classification adopted here is rather traditional and
Reig (1958) proposed the subordinal ñames Archaeo- generally follows that of the most recent checklist of anu-
batrachia and Neobatrachia to include fundamentally those rans (D. Frost, 1985) in the recognition of families, except
groups of anurans that had been referred to as archaic that arthroleptines and hemisines are regarded as
and advanced, respectively. Both Noble (1922, 1931b) subfamilies of the Ranidae rather than sepárate families.
and J. D. Lynch (1973) posited that some families could No superfamilies are recognized.
be regarded as transitional between these two categories. Contení.—Twenty-one living and one extinct family
Duellman (1975) employed Reig's subordinal classifica- are recognized. These contain 301 living genera with 3438
tion and recognized six superfamilies; these also were species, plus 98 extinct species. Including those fossil
used by Laurent (1979) and with slight modification by genera not assigned to family, there are 38 extinct genera
Dubois (1983) (Table 19-1). Sokol (1977a) recognized with 64 species.
two suborders, the Discoglossoidei and the Ranoidei, based
on sepárate trigeminal and facial ganglia and free ribs in LEIOPELMATIDAE Mivart, 1869
the former and fused ganglia and no ribs in the latter. As Deflnition.—There are nine ectochordal, presacral
a compromise between the classificattons of Duellman vertebrae with cartilaginous intervertebral joints and non-
(1975) and Sokol (1977a), Laurent (1979) proposed the imbricate neural arches. Presacrals I and II are not fused,
subordinal ñame Mesobatrachia to include parí of the and the atlantal cotyles of Presacral I are closely juxta-

Table 19-1. Comparison of Three Recent Classifications of Anurans

Duellman (1975) Laurent (1979) Dubois (1983)

Suborder Archaeobatrachia Suborder Archaeobatrachia Suborder Discoglossoidei
Superfamily Discoglossoidea Superfamily Discoglossoidea Superfamily Discoglossoidea
Family Leiopelmatídae Family Leiopelmatídae Family Discoglossidae
Discoglossidae Discoglossidae Leiopelmatídae
Superfamily Pipoidea Suborder Mesobatrachia Suborder Pipoidei
Family tPalaeobatrachidae Superfamily Pipoidea Superfamily Pipoidea
Pipidae Family Pipidae Family Pipidae
Rhinophrynidae tPalaeobatrachidae Rhinophrynidae
Superfamily Pelobatoidea Rhinophrynidae Superfamily Pelobatoidea
Family Pelobatídae Superfamily Pelobatoidea Family Pelobatídae
Pelodytidae Family Pelobatidae Pelodytidae
Suborder Neobatrachia Pelodytidae Superorder Ranoidei
Superfamily Bufonoidea Suborder Neobatrachia Superfamily Hyloidea
Family Myobatrachidae" Superfamily Bufonoidea Family Rheobatrachidae
Leptodactylidae Family Rheobatrachidae Myobatrachidae
Bufonidae Myobatrachidae Sooglossidae
Brachycephalidae Sooglossidae Leptodactylidae
Rhinodermatídae Leptodactylidae Dendrobatidae
Dendrobatidae Phyllobatídae'1 Bufonidae
Pseudidae Bufonidae Brachycephalidae
Hylidaec Brachycephalidae Rhinodermatidae
Centrolenidae Rhinodermatidae Pseudidae
Superfamily Microhyloidea Pseudidae Hylidae
Family Microhylidae Hylidae Centrolenidae
Superfamily Ranoidea Centrolenidae Pelodryadidae
Family Sooglossidae Pelodryadidae Superfamily Microhyloidea
Ranidaed Superfamily Microhyloidea Family Microhylidae
Hyperoliidae Family Microhylidae Superfamily Ranoidea
Rhacophoridae Superfamily Ranidae6 Family Ranidae
Family Hyperoliidae' Rhacophoridae
Ranidae Arthroleptidae
Hemisidae Hyperoliidae
Hemisidae
"Includes Rheobatrachidae. dlncludes Arthroleptidae and Hemisidae.
'"Equals Dendrobatidae. Includes Rhacophoridae.
clncludes Pelodryadidae. 'Includes Arthroleptidae.
 Classification
517

Figure 19-25. A. Ascaphus truel

from Mount Ranier, Washington,
U.S.A. (photo by J. T. Collins).
B. Leiopelma hochstetteri from New
Zealand (photo by J. V. Vindum).

Figure 19-26. Distribution of living

members of the family
Leiopelmatidae (North America and
New Zealand), Discoglossidae
(Eurasia and North África), and
Rhinophrynidae (North and Central
America).

posed. Free ribs are present on Presacrals II-IV and oc- diploid chromosome complement varíes from 5 pairs of
casionally on Presacral V in adults (on Presacrals II-V macrochromosomes and 18 pairs of microchromosomes
and occasionally on Presacral VI in Notobatrachus). The (Ascaphus) to 11 pairs of macrochromosomes and 0-8
sacrum has narrowly dilated diapophyses and has a con- pairs of microchromosomes (Leiopelma).
tiguous cartílaginous connection with the coccyx, which Living leiopelmatids are small frogs attaining snout-
has transverse processes proximally. The pectoral girdle vent lengths of no more than 50 mm. However, the Jur-
is arciferal and has a cartilaginous omosternum and ster- assic Notobatrachus attained 150 mm, and a subfossil
num; the anterior end of the scapula is overlain by the Leiopelma had a snout-vent length of about 100 mm.
clavicle in Ascaphus but not in Leiopelma or Notobatra- The terrestrial Leiopelma and the aquatic Ascaphus are
chus. Palatines are absent; a parahyoid bone is present, dull gray or brown and have little webbing on the feet
and the cricoid ring is complete. The maxillae and pre- (Fig. 19-25). Living leiopelmatids are unique among anu-
maxillae are dentate. The astragalus and calcaneum are rans in having vestigial tail-wagging muscles (m. cauda-
fused only proximally and distally; there are three tarsalia, liopuboischioübialis); Ascaphus is unique in having an
and the phalangeal formula is normal. The m. sartorius intromittent organ formed from a cloacal extensión in
is not discrete from the m. semitendinosus, and the ten- males, and Leiopelma is unique among amphibians in
dón of the latter inserts ventral to the m. gracilis; the m. possessing cartilaginous inscriptional ribs.
glutaeus magnus lacks an accessory tendón, and the m. Distribution.—Living leiopelmatids occur only in New
adductor magnus lacks an accessory head. The pupil is Zealand, where they are the only naüve anurans, and in
vertically elliptical. Amplexus is inguinal. Development is northwestern United States and extreme southwestern
direct in Leiopelma. The aquatic Type III larvae of As- Canadá (Fig. 19-26).
caphus have beaks and many rows of denudes; a single Fossil history.—The family is known from two extinct
median spiracle is formed by a hiatus in the operculum, genera from the Jurassic of Patagonian Argentina.
and the trigémina! and facial ganglia are sepárate. The Life history.—Ascaphus deposits unpigmented eggs in
EVOLUTION
strings adherent to undersides of rocks in mountain proximally and distally; there are three tarsalia, and the
streams; the tadpoles develop in torrenüal streams and phalangeal formula is normal. The m. sartorius is not
have an oral disc and up to 16 rows of denticles. Leío- discrete from the m. semitendinosus, and the tendón of
pe/ma deposits large, unpigmented eggs encased in a the latter inserís ventral to the m. gracilis; the m. glutaeus
membrane in damp terrestrial situaüons; the eggs undergo magnus lacks an accessory tendón (present and fleshy in
direct development. Barbourula and Bombina), and the m. adductor magnus
Remarfcs.—Some workers have used the familial ñame lacks an accessory head. The pupil is vertically elliptical
Ascaphidae dating from Fejérváry, 1923. J. Savage (1973) in Alytes and triangular in the others. Amplexus is in-
recognized both families, one for each of the living gen- guinal. All have aquatic Type III larvae with beaks and
era. Even though tríese genera are associated principally denticles; a single median spiracle is formed by a hiatus
by primitive character states, their recognition as distri- in the operculum, and the trigeminal and facial ganglia
buüonal relicts of a single formerly widespread group is are sepárate. The diploid chromosome complement var-
supported by the presence of fossils in Jurassic forma- íes from 22 to 28 macrochromosomes; 8 pairs of micro-
tions in Argentina (Estes and Reig, 1973). chromosomes in A/yíes give a total complement of 38.
Contení.—The two living genera contain four species; Living discoglossids vary from the small (40-50 mm
two extinct species are placed in two other genera: in snout-vent length) toadlike A/y£es, Baleaphryne, and
Bombina to the large (85-mm) aquatic Barbourula with
1. Ascaphus Stejneger, 1899; 1 species. North- webbed hands and feet (Fig. 19-27). The species of
western United States and adjacent Canadá. Bombina have black mottling on a bright orange or yel-
Metter (1968b). low venter.
2. Leiopelma Fitzinger, 1861; 3 species. New Distribution.—The distribution of living discoglossids
Zealand. B. Bell (1978). is disjunct in Eurasia and adjacent regions. The major
3. Wotobatrachus Reig, 1957; 1 species. Late distribution of the family includes Europe eastward through
Jurassic of Argentina. Estes and Reig (1973). Turkey, Israel, and Syria to western U.S.S.R., plus North
4. tV¡erae//a Reig, 1961; 1 species. Early Jurassic África. Bombina also occurs in eastern U.S.S.R., China,
of Argentina. Estes and Reig (1973). Vietnam, and Korea, and Barbourula is known from the
Philippines and Borneo (Fig. 19-26).
DISCOGLOSSIDAE Günther, 1859 Fossil history.—The family is comparatively well rep-
Definition.—There are eight stegochordal, opistho- resented by fossils from Europe (Upper Jurassic through
coelous presacral vertebrae with imbrícate neural arches. Quatemary) and North America (Upper Cretaceous and
Presacrals I and II are not fused, and the atlantal cotyles Paleocene). The family also is known from the upper
of Presacral I are closely juxtaposed. Free ribs are present Eocene of England and the middle Miocene of the Cau-
on Presacrals II-IV. The sacrum has expended di- casus Mountains. Eight extinct genera are recognized;
apophyses and a bicondylar articulation with the coccyx four Recent genera are represented in the fossil record.
(monocondylar in Barbouruta), which has transverse Life history.—Insofar as is known, all discoglossids have
processes proximally. The pectoral girdle is arciferal and aquatic eggs and larvae. Bombina lays pigmented eggs
has a cartilaginous omosternum (greatly reduced in Bom- singly in ponds, and Discog/ossus deposits clumps of pig-
bina and Discog/ossus) and sternum; the anterior end of mented eggs in ponds. Barbourula has unpigmented eggs
the scapula is overlain by the clavicle. Palatinos are ab- and presumably deposits them in streams. Alytes mates
sent; a parahyoid bone (or bones) is present, and the on land. The eggs are exuded in strings; subsequent to
cricoid ring is complete. The maxillae and premaxillae fertilization, the amplectant male shifts to a cephalic em-
are dentate. The astragalus and calcaneum are fused only brace and pushes his legs among the eggs until they

Figure 19-27. A. Alytes

obstetrícans, male carrying eggs.
from Provincia Oviedo, Spain.
B. Discoglossus pictus from
Provincia Cádiz, Spain. Photos by S.
D. Busack.
 Classification
adhere to his back and thighs. The male carnes the eggs 519
(into and out of water) unül they are ready to hatch, at
which time he enters the water. The tadpoles of Barbou-
ruh are unknown; otherwise, discoglossid tadpoles are a
generalized pond-type with two upper and three lower
rows of denudes.
Remarfcs.—The family is associated with the Leiopel-
matidae on the basis of plesiomorphic characters and two
synapomorphies of the larvae: (1) extensive fusions among
hyobranchial elements, and (2) operculum greatly elon-
gated posteriorly with a single midventral spiracular opening
(Sokol, 1975). Lanza et at (1976) showed that Disco-
g/ossus was immunologically distant from Bombina and
A/ytes and suggested that the latter two genera should
be placed in a sepárate family, the Bombinidae. (Bar-
bouru/a was not compared, and Ba/eaphryne was un- Figure 19-28. Rhinophrynus dorsalis from Campeche, México.
Photo by J. T. Collins.
known at the time.) Estes and Sanchíz (1982) discussed
intrafamilial relaüons and retained all of the genera in
one family.
Contení.—Fourteen living species are placed in five 10. tPe/ophi/us Tschudi, 1838; 1 species. Middle
genera. Eleven species are recognized in eight extinct Miocene of Germany.
genera: 11. tProdiscog/ossus Friant, 1944; 1 species. Oli-
gocene of France.
1. A/ytes Wagler, 1830 (Obstetricans Dugés, 12. tScoíiophryne Estes, 1969; 1 species. Upper
1834; Ammoryctis Lataste, 1879); 2 spe- Cretaceous and middle Paleocene of Mon-
cies. Western, central, and southern Europe, tana and Wyoming, U.S.A.
and northwestem África. Upper Miocene and 13. tSpondy/ophryne Kretzoi, 1956; 1 species.
Pleistocene of western Europe. Crespo Pleistocene of Hungary.
(1979).
2. Baleaphryne Sanchíz and Alcover, 1977; 1 RHINOPHRYNIDAE Günther, 1859
species. Mallorca, Balearte islands, Spain. Deflnition.—There are eight, ectochordal, modified
Pleistocene of Mallorca and Minorca, Spain. opisthocoelous presacral vertebrae (the intervertebral body
Hemmer and Alcover (1984). tends to adhere to the anterior end of the centrum, but
3. TBaranophrys Kretzoi, 1956; 1 species. Pleis- is not fused to it) with imbrícate neural arches. Presacrals
tocene of Hungary. I and II are not fused, and the atlantal cotyles of Presacral
4. Barbourula Taylor and Noble, 1924; 2 spe- I are closely juxtaposed. Free ribs are absent. The sacrum
cies. Palawan, Philippine Islands, and north- has expanded diapophyses and a bicondylar articulation
ern Borneo. with the coccyx, which lacks transverse processes. The
5. Bombina Oken, 1816 (Bombinator Merrem, pectoral girdle is arciferal and lacks an omostemum and
1820); 6 species. Europe, Turkey, and west- sternum; the anterior end of the scapula is overlain by
ern U.S.S.R.; eastern Asia, including the clavicle. Palatines are absent; a parahyoid bone is
U.S.S.R., China, Korea, and Vietnam. Mid- present, and the cricoid ring is incomplete dorsally. The
dle Miocene through Pleistocene of Europe. maxillae and premaxillae are edentate. The astragalus
6. Discog/ossus Otth, 1837 (Pseudes Wagler, and calcaneum are fused only proximally and distally;
1834; Co/odacry/us Tschudi, 1845); 3 spe- there are two tarsalia, and the phalangeal formula is nor-
cies. Southern Europe, northwestem África, mal except for the loss pf one phalange on the first toe.
Israel, and Syria. Miocene through the Pleis- The m. sartorius is distínct from the m. semitendinosus,
tocene of southern Europe. and the tendón of the latter penetrales the m. gracilis;
7. tEodiscog/ossus Villada, 1957; 1 species. Up- the m. glutaeus magnus has no accessory tendón, and
per Jurassic and Lower Cretaceous of Spain. the m. adductor magnus has no accessory head. The
Estes and Sanchíz (1982). pupil is vertical. Amplexus is inguinal. The aquatic Type
8. tLcitonia Meyer, 1843 (tDip/ope/turus De- I larvae have no beaks or denudes; paired, ventrolateral
peret, 1897; tMiope/obates Wettstein-Wes- spiracles are formed as hiatuses in the operculum, and
tersheimb, 1955); 4 species. Miocene of Eu- the trigeminal and facial ganglia are fused. The diploid
rope. chromosome complement is 22.
9. tParadiscog/ossus Estes and Sanchíz, 1982; This fossorial, toadlike anuran has a robust body, short
1 species. Upper Cretaceous of Wyoming, limbs, smooth skin, minute head, and a body length of
U.S.A. about 75 mm (Fig. 19-28). The inner metatarsal rubercle
EVOLUTION
520 js enlarged and spadelike; the frogs dig into soil rapidly barbéis and may have had paired spiracles (interpreta-
by lateral movements of the feet. Rhinophrynus may be tíons vary).
unique among anurans in having a tongue that is cata- Palaeobatrachids were Xenopus- like aquatic frogs with
pulted out of a small mouth; the small, pointed snout is fully webbed feet. Some species attained a snout-vent
calloused. length of 120 mm. The teeth are elongate and nonpedi-
Distribution.—This family inhabits subhumid lowland cellate.
áreas from southern Texas, U.S.A., and Michoacán, Fossil history.—Palaeobatrachids are well repre-
México, to Costa Rica (Fig. 19-26). sented in the fossil beds from the Eocene through the
Fossíí history.—Rhinophrynids are known from the Pliocene of Europe; specimens from the Upper Jurassic
late Paleocene and middle Eocene of Wyoming and the and the Pleistocene of Europe also are referred to this
early Oligocene of Saskatchewan, Canadá. family. Upper Cretaceous specimens from North America
Life history.—Rhinophrynus spends most of its life formerly referred to the discoglossid genus Barbourula
underground. The frogs emerge only after heavy rains. are palaeobatrachids (Estes and Sanchíz, 1982).
Males cali while floating on the surface of temporary ponds; Remarks.—Palaeobatrachids apparently are the sister
the vocal sacs are paired and internal. Eggs are deposited group of the Pipidae, from which they differ by having
in masses and subsequently float singly to the surface. procoelous, instead of opisthocoelous, vertebrae and an
The pelagic, filter-feeding tadpoles have 11 barbéis (Fig. extra phalange on the fifth toe (Estes and Reig, 1973).
6-14B). The family has been studied extensively by Spinar (1972),
Remarks.—Rhinophrynids are considered to be the and much more material now is available from the Messel
sister group of the pipids and palaeobatrachids; this re- Quarry in Germany.
lationship is based mainly on larval characters of pipids Contení.—At least 17 species in five extinct genera are
and rhinophrynids (Sokol, 1975). However, on the basis recognized:
of phenetic immunological distance, Maxson and Daugh-
erty (1980) suggested that Rhinophrynus was more closely, 1. TAlbionbatrachus Meszoely, Spinar, and Ford,
albeitstill distantly, related to Ascaphus (Leiopelmatidae). 1984; 1 species. Eocene of Isle of Wight, Eng-
Contení.—A single living genus contains one living and land.
one extinct species; another species is placed in an extínct 2. 1l.it/iobairac/ius Parker, 1929; 1 species. Lower
genus: Miocene of Europe. Sanchíz (1981).
3. 'fNeusibatmchus Seiffert, 1972; 2 species. Ju-
1. tEorhinophrynus Hecht, 1959; 1 species. Late rassic-Cretaceous boundary of Spain and
Paleocene and middle Eocene of Wyoming, Miocene of Czechoslovakia.
U.S.A. 4. tPa/aeobatrachus Tschudi, 1838 (tPa/aeo-
2. Rhinophrynus Duméril and Bibron, 1841; 1 phrynos Giebel, 1850; tPe/obatinopsis Kuhn,
species. Rio Grande Embayment of Texas and 1941; TQuinquevertebron Kuhn, 1941); 12
Michoacán, México, southward to Costa Rica. species. Eocene through Pliocene of Europe.
One fossil species from the early Oligocene Spinar (1972).
of Saskatchewan, Canadá. Fouquette (1969). 5. tP/iobaírachus Fejérváry, 1917; 1 species.
Pleistocene of Germany. Sanchíz and Mly-
tPALAEOBATRACHIDAE Cope, 1865 narski (1979).
Definition.—(Data incomplete). There are seven or eight
stegochordal, procoelous presacral vertebrae with imbrí- PIPIDAE Gray, 1825
cate neural arches; the last two presacral vertebrae are Definition.—There are 6-8 epichordal, opisthocoe-
fused with the sacrum in some specimens. Presacrals I lous, presacral vertebrae with imbrícate neural arches.
and II are fused, and the atlantal cotyles of Presacral I Presacrals I and II are fused (unfused ¡n Xenopus), and
are juxtaposed. Ribs are free in subadults and ankylosed the atlantal cotyles of Presacral I are juxtaposed (sepárate
to the transverse processes of Presacrals II-VI ¡n adults. in Pipa). Presacral VIII is fused with the sacrum ¡n some
The sacrum has dilated diapophyses and a bicondylar Pipa. The ribs are free in subadults of living genera and
articulation with the coccyx, which lacks transverse in adults of Early Cretaceous taxa, but are ankylosed to
processes (present proximally in some subadults). The the transverse processes of Presacrals II-IV in adults of
pectoral girdle is arciferal; the anterior end of the scapula living taxa. The sacrum has expanded diapophyses and
is overlain by the clavicle. Palatines are absent; a para- is fused with the coccyx, which usually lacks proximal
hyoid bone is present. The maxillae and premaxillae are transverse processes free of the sacrum. The pectoral
dentate. The astragalus and calcaneum are fused only girdle is pseudofirmisternal and lacks an omosternum.
proximally and distally; there are two tarsalia, and the The sternum is greatly expanded, and the epicoracoid
phalangeal formula is normal for the hand but increased cartilages are elaborated posterior to the coracoids. The
in the foot by the addition of an extra phalange in the clavicle and scapula are fused, except in most Pipa, in
fifth toe. Aquatic Type I larvae had at least three pairs of which the anterior end of the scapula is overlain by the
 Classificatíon
521

Figure 19-29. A. Xenopus gil/i from

Cape Fíats, South África (photo by
J. Visser). B. Pipa pipa from
Surinam (photo by K. T. Nemuras).

Figure 19-30. Distribution of living

members of the family Pipidae in
South America and África and the
family Pelodytidae in Europe and
southwestern Asia.

clavicle. Palatines are absent; a parahyoid is absent, and Lateral-line organs are present (except in Hymenochirus
the cricoid ring is complete. The maxillae and premaxillae and Pseudhymenochirus,); the eyes are small and dorsal,
have nonpedicellate teeth in Xenopus and some species and eyelids are poorly developed or absent. The range
of Pipa, and they are edentate in other species of Pipa, in size of living pipids is contained within the genus Pipa—
Hymenochirus, and Pseudhymenochirus. The astragalus 44 mm in P. parva to 171 mm in P. pipa. Pipids are
and calcaneum are fused only proximally and distally; unique among frogs in lacking a tongue.
there are two tarsalia, and the phalangeal formula is nor- Distribution.—The range of the family is disjunct; it
mal. The m. sartorius is not discrete from the m. semi- occurs in tropical South America east of the Andes and
tendinosus (partially sepárate in Xenopus), and the ten- in adjacent Panamá and in sub-Saharan África (Fig. 19-
dón of the latter penetrates the m. gracilis; the m. glutaeus 30).
magnus has an accessory tendón, and the m. adductor Fossil history.—Pipids are better represented in the
magnus lacks an accessory head. The pupil is round. fossil record than most families of anurans (see Báez,
Amplexus is inquinal. The aquatic Type I larvae lack beaks 1981, for review). They are known from the Lower Cre-
and denudes; paired, ventrolateral spiracles are formed taceous of Israel, Upper Cretaceous through the Miocene
as hiatuses in the operculum (spiracles absent in Hy- of África, and the Upper Cretaceous and Paleocene of
menochirus), and the trigémina! and facial ganglia are South America.
fused. The diploid chromosome complement is 20-36; Life history.—African pipids deposit small, pigmented
some species of Xenopus (2 N = 36) are polyploids. eggs on vegetation or as a surface film in quiet water;
These strictly aquatic frogs have long, unwebbed fin- the tadpoles have a single pair of barbéis (Fig. 6-14A)
gers (webbed in Hymenochirus and Pseudhymenochi- and are pelagic filter-feeders (except Hymenochirus which
rus) and large, fully webbed feet; in all except Pipa, the lacks barbéis and is carnivorous). In Pipa, the eggs are
toes termínate in clawlike, keratinized tips (Fig. 19-29). imbedded in the dorsal skin of the female; in some spe-
EVOLUTION
522 Cies (e g^ p cawalhoi) the eggs hatch into filter-feeding megophryines). Presacrals I and II are not fused, and the
tadpoles, and in others (e.g., P. pipa) the eggs develop atlantal cotyles of Presacral I are closely juxtaposed. Ribs
directly into froglets. Hymenochirus and Pipa have a are absent. The sacrum has greatly expanded diapoph-
complex courtship involving aquaüc acrobatics (see yses and ¡s fused with the coccyx (monocondylar artic-
Chapter 3). ulation with the coccyx in most megophryines and some
Remarks.—Some authors (e.g., Dubois, 1983) rec- eopelobatines). Transverse processes on the proximal part
ognize two subfamilies—the Pipinae for the South Amer- of the coccyx possibly are incorporated into a bony web
ican Pipa and the Xenopinae (or the Dactylethrinae) for between the coccyx and the sacral diapophyses in some
the African genera. Although larval African pipids share taxa. The pectoral girdie is arciferal and has a cartilagi-
four synapomorphies, the adults of Hymenochirus are nous omosternum and sternum (latter osseous in most
divergent from other pipids (Sokol, 1977b); moreover, taxa); the anterior end of the scapula is not overlain by
the división of the Pipidae does not take into account the the clavicle. Palatines are present, absent, or fused with
diverse fossil pipids, which include nominal Xenopus in adjacent elements; a parahyoid is absent, and the cricoid
South America. ring is incomplete dorsally. The maxillae and premaxillae
Contení.—Four extant genera contain 26 living spe- are dentate. The astragalus and calcaneum are fused only
cies. Six extinct species are grouped into five genera, and proximally and distally; there are two tarsalia, and the
six others are placed in the extant genus Xenopus: phalangeal formula is normal. The m. sartorius ¡s not
discrete from the m. semitendinosus, and the tendón of
1. tCordicepha/us Nevo, 1968; 2 species. Lower the latter inserts ventral to the m. gracilis; the m. glutaeus
Cretaceous of Israel. Nevo (1968). magnus has an accessory tendón, and the m. adductor
2. tEoxenopoides Haughton, 1931; 1 species. magnus lacks an accessory head. The pupil is vertically
Upper Eocene or Oligocene of South África. elliptical. Amplexus is inguinal. All have aquatic Type IV
Estes (1977). larvae with beaks and denudes; the spiracle is sinistral,
3. Hymenochirus Boulenger, 1896; 4 species. and the trigémina! and facial ganglia are fused. The dip-
Equatorial western África. Perret (1966). loid number of chromosomes is 26 (24 in Leptolalax
4. Pipa Laurenü, 1768 (Pipona Rafinesque, 1815; pelodytoides).
Asterodactylus Wagler, 1830; Leptopus Mayer, The holarctic pelobatines are short-legged, smooth-
1835; Protopipa Noble, 1925; Hemipipa Mi- skinned fossorial toads with spadelike metatarsal tuber-
randa-Ribeiro, 1937); 7 species. Northern cles; the largest attain a snout-vent length of about 85
South America east of the Andes; eastern mm. The Oriental megophryines are more diverse in ex-
Panamá. Trueb (1984). ternal appearance; they are terrestrial or semifossorial,
5. Pseudhymenochirus Chabanaud, 1920; 1 spe- and some have fleshy dorsolateral folds and/or suprac-
cies. Western África ¡n Guinea and Sierra iliary processes (Fig. 19-31). The largest megophryines
Leone. have a snout-vent length of about 125 mm.
6. tSa/tenia Reig, 1959; 1 species. Upper Cre- Distríbution.—Megophryines are distributed from
taceous of Argentina. Báez (1981). Pakistán east to western China and through the Indo-
7. tShomrone//a Estes, Spinar and Nevo, 1978; Australian Archipelago to the Sunda Islands and the Phil-
1 species. Lower Cretaceous of Israel. Estes ippine Islands. Pelobatines occur in Europe, western Asia,
et al. (1978). North África, and southern North America to southern
8. tThorad/iacus Nevo, 1968; 1 species. Lower México (Fig. 19-32).
Cretaceous of Israel. Nevo (1968). Fossil history.—Pelobatids have an extensive fossil
9. Xenopus Wagler, 1827 (Dactylethra Cuvier, history extending from the Late Cretaceous of North
1829; Silurana Gray, 1864; tShe/ania Casa- America and Asia and from the middle Eocene of Europe
miquela, 1961; tLibycus Spinar, 1980); 14 through the Pleistocene.
species. Sub-Saharan África. Two fossil spe- Life history.—All pelobatids have aquatic eggs and
cies in South America (middle or upper Pa- tadpoles. Pelobatines and some megophryines deposit
leocene of Brazil, upper Paleocene of Argen- pigmented eggs in temporary ponds and have general-
tina) and four species in África (Upper ized pond-type tadpoles. Other megophryines (Lepto-
Cretaceous of Niger, Oligocene of Libya, brachium, Leptolalax, and Scutiger) have stream-adapted
Miocene of Morocco and South África) (Estes, tadpoles, and the tadpoles of Megophrys are surface-
1975; Tinsley, 1981). feeders with upturned, funnel-shaped mouths (Figs. 6-
12B, 6-13B).
PELOBATIDAE Bonaparte, 1850 Remarks.—The recognitíon of one extinct and two
Deflnition.—There are eight stegochordal presacral living subfamilies is based primarily on the work of Estes
vertebrae with imbrícate neural arches. Ossified interver- (1970). Some workers include the pelodytids as a
tebral discs are present; these fuse with the centrum to subfamily of the Pelobatidae. Rocek (1981) suggested
give a procoelous centrum in adults (discs remain free in that Pelobates and Scaphiopus evolved independenth
 Classification
523

Figure 19-31. A. Megophrys

montana from Asia (photo by K. T.
Nemuras). B. Scaphiopus
bombifrons from Comanche County,
Kansas, U.S.A. (photo by J. T.
Collins).

Figure 19-32. Distribution of living

members of the family Pelobatidae.

and represented two families, but the immunological re- Cretaceous of Mongolia and southwestern
sults of Sage et al. (1982) purport to show that the two Asia. Estes (1970); Rocek (1981).
genera were related but that their differenüation occurred 3. tKizy/kuma Nessov, 1981; 1 species. Late
in the Cretaceous. Cretaceous of Ubekistan, U.S.S.R.
Contení.—Nine Recent genera containing 83 living MEGOPHRYINAE Noble, 1931
species, are placed in two subfamilies, one of which con- 4. Atympanop/irys Tian and Hu, 1983; 1 spe-
tains a monotypic extinct genus. Three other extinct gen- cies. Sichuan, China. Tian and S. Hu (1983).
era containing 12 species is placed in a third subfamily. 5. Bmchytarsophrys Tian and Hu, 1983; 1 spe-
Eight other fossil species are contained in one of the living cies. Southwestern China, Burma, and
genera. northern Thailand. Tian and S. Hu (1983).
6. Leptobrachella Smith, 1931 (Nesobia van
tEOPELOBATINAE Spinar, 1972 Kampen, 1923); 6 species. Borneo and Ña-
1. tAra/obatrachus Nessov, 1981; 1 species. Late tuna islands. Dring (1984).
Cretaceous of Ubekistan, U.S.S.R. 7. Leptobrachium Tschudi, 1838 (Septobrach-
2. tEope/obaíes Parker, 1929 (tHa//eobatra- ium Tschudi, 1838; Pelobatrachus Beddard,
chus Kuhn, 1941; tEobu/e//a Kuhn, 1941; 1907; Vibrissaphora Liu, 1945); 11 species.
tParabu/e//a Kuhn, 1941; tPa/aeope/obates Southern China and Indochina, Philippines,
Kuhn, 1941; tArchaeope/obates Kuhn, 1941; Sunda Islands to Bali.
tAmphignat/iodontoides Kuhn, 1941; 8. Leptolalax Dubois, 1980 (Carpophrys Her-
tGermanobatrachus Kuhn, 1941); 10 spe- petol. Dept. Sichuan Biol. Res. Inst., 1977);
cies. Late Cretaceous (?), early Eocene to 4 species. Southern China to Malaya and
early Oligocene of North America; middle Borneo.
Eocene to middle Miocene of Europe; Late 9. Megophrys Kuhn and van Hasselt, 1822
EVOLUTION
524 (Megalophrys Wagler, 1830; Ceratophryne tate. The astragalus and calcaneum are completely fused;
Schlegel, in Günther, 1859; Xenop/irys there are three tarsalia, and the phalangeal formula is
Günther, 1864; Ophryophryne Boulenger, normal. The m. sartorius is not discrete from the m. semi-
1883); 21 species. Southeastern Asia from tendinosus, and the tendón of the latter inserís ventral to
India to China; Philippines, Sumatra, Java, the m. gracilis; the m. glutaeus magnus has an accessory
Borneo, and Natuna. tendón, and the m. adductor magnus lacks an accessory
10. Scutiger Theobold, 1868 (Cophophryne head. The pupil is vertically elliptical. Amplexus is in-
Boulenger, 1903; Aelurophryne Boulenger, guinal. The aquatic Type IV larvae have beaks and den-
1919; Oreolalax Myers and Levitón, 1962); udes; the spiracle is sinistral, and the trigémina! and facial
29 species. Mountains of southwestem China ganglia are fused. The diploid number of chromosomes
to northern India. is24.
PELOBATINAE Bonaparte, 1850 Pelodytids are smooth-skinned, toadlike fossorial anu-
11. tMacrope/obates Noble, 1924; 1 species. rans. The máximum size is about 50 mm (Fig. 19-33).
Middle Oligocene of Mongolia. Estes (1970). Distribution.—The distribution is disjunct in western
12. Pelobates Wagler, 1830 (Cu/íripes Müller, Europe and southwestem Asia (Fig. 19-30).
1832; Didocus Cope, 1866; tZaphrissa Cope, Fossil history.—Pelodytids are known from the mid-
1866; tProíope/obates Bieber, 1880; Pseu- dle Eocene through the Pleistocene of Europe (Sanchíz,
dopelobates Pasteur, 1958); 4 species. Eu- 1978) and from the Miocene of North America.
rope, western Asia, and northwestern África. Life history.—Pigmented eggs are laid in strings in
Middle Eocene to Pleistocene of Europe. ponds. The larvae are generalized pond-type tadpoles.
13. Scaphiopus Holbrook, 1836 (Spea Cope, Remarks.—Pelodytids are placed as a subfamily of the
1866; -fNeoscaphiopus Taylor, 1942); 6 Pelobatidae by some workers. Pelodytids differ from pe-
species. North America. Early Oligocene lobatids in having Presacrals I and II fused, a parahyoid
through Pleistocene of North America (8 ex- bone, fused astragalus and calcaneum, and three tarsalia.
tinct species). Kluge (1966). Contení.—Two Recent species are in one genus; two
monotypic extinct genera are recognized:
PELODYTIDAE Bonaparte, 1850
Deflnition.—There are eight stegochordal presacral 1. tMiope/odyíes Taylor, 1942; 1 species. Middle
vertebrae with procoelous centra and imbrícate neural Miocene of Nevada, U.S.A.
arches. The arches of Presacrals I and II are fused, and 2. Pelodytes Fitzinger, in Bonaparte, 1838 (Pe-
the atlantal cotyles of Presacral I are closely juxtaposed. ¡odytopsis Nikolski, 1896); 2 species. Western
Ribs are absent. The sacrum has broadly dilated dia- Europe and Caucasus Mountains of south-
pophyses and has a bicondylar articulatíon with the coc- westem Asia, middle Eocene of Germany,
cyx, which bears transverse processes proximally. The middle Miocene of Spain, and Pleistocene of
pectoral girdle is arciferal and has a cartílaginous omos- France.
ternum and osseous sternum; the anterior end of the 3. tPrope/odytes Weitzel, 1938; 1 species. Eocene
scapula is not overlain by the clavicle. Palatínes are present; of Germany.
a parahyoid bone is present, and the cricoid ring is in-
complete dorsally. The maxillae and premaxillae are den- MYOBATRACHIDAE Schlegel, 1850
Definition.—There are eight presacral vertebrae with
a persisten! notochord and free intervertebral discs in
•;f
subadults (except free discs absent in Lechriodus and
Mixophys) that tend to be fused to the posterior end of
the sacrum in adults (procoely). The neural arches are
imbrícate in most limnodynastínes and nonimbricate in
most myobatrachines. Presacrals I and II are fused in
limnodynastínes (except Lechriodus and Mixophys) and
are not fused in myobatrachines. The atlantal cotyles of
Presacral I are juxtaposed in limnodynastínes and widely
separated in myobatrachines. Ribs are absent. The sa-
crum has dilated diapophyses and has a bicondylar ar-
tículation with the coccyx, which may or may not have
transverse processes proximally. The pectoral girdle is
arciferal and has a cartílaginous omosternum (absent in
Myobatrachus and Notaden) and sternum. The anterior
Figure 19-33. Pelodytes punctatus from Provincia Cádiz, Spain. end of the scapula is not overlain by the clavicle. Pala-
Photo by S. D. Busack. tines are present; a parahyoid is absent, and the cricoid
 Classification
525

Figure 19-34. A. Rheobatrachus

si/us from Queensland, Australia.
B. Mixophys iteratus from
Queensland, Australia. C.
Limnodynostes terrareginae from
Queensland, Australia. D. Notaden
melanoscaphus from Western
Australia. Photos by W. E. Duellman.

ring is complete in limnodynastines and incomplete ven- Distribution.—All living genera inhabit Australia; three
trally in myobatrachines. The maxillae and premaxillae genera also occur on New Guinea and four on Tasmania
are dentate in most genera (edentate in Myobatrachus, (Fig. 19-35).
Notaden, Pseudophryne, and some Uperoleia). The as- Fossil history.—The Eocene /ndobatrachus tenta-
tragalus and calcaneum are fused only proxirnally and tívely was referred to this family by J. D. Lynch (1971).
distally; there are two tarsalia, and the phalangeal for- Limnodynastes is known from the Miocene, and it and
mula is normal. The m. sartorius usually is distinct from two other genera are known from the Pleistocene of Aus-
the m. semitendinosus, and the place of inserüon of the tralia.
tendón of the latter is variable (ventral to m. gracilis in Life history.—Eggs are laid on land by members of
most limnodynastines, penetraüng m. gracilis in other several genera; most of these develop into aquatic tad-
limnodynastines and some myobatrachines, and dorsal poles, but nonfeeding tadpoles develop in the nests of
to m. gracilis in other myobatrachines); the m. glutaeus Kyarranus and Philoria and in brood pouches in the male
magnus has an accessoty tendón, and the m. adductor of Assa, and terrestrial eggs undergo direct development
magnus has a small accessory head. The pupil usually is in Arenophryne and Myobatrachus. The eggs and tad-
horizontal (vertically elliptical in Heleioporus, Megistolo- poles are brooded in the stomach of Rheobatrachus.
tis, Mixophys, and Neobatrachus). Amplexus is inguinal. Aquatic foam nests are characteristic of some limnody-
In those species having aquatic larvae, they are Type IV nastines, whereas other myobatrachids deposit their eggs
with beaks and denticles; the spiracle is sinistral, and the in water; in both cases the larvae are aquatic. Megisío/otis
trigeminal and facial ganglia are fused. The diploid chro- has tadpoles adapted for torrential streams.
mosome complement is 24, except that four species of Remarles.—Many authors (e.g., Tyler, 1979) include
Limnodynastes have 22. the myobatrachids in the Leptodactylidae. J. D. Lynch
Myobatrachids are extremely variable in size; Asso dar- (1973) included the African He/eophryne (now recog-
Hngtoni attains a snout-vent length of only 20 mm, whereas nized in its own family) as a subfamily of the Myobatrach-
Mixophys iteratus reaches 115 mm. Most myobatrachids idae, in which he recognized the Cycloraninae and
are terrestrial, and some (notably Arenophryne, Myo- Myobatrachinae. Cyc/orana has been transferred to the
batrachus, and Notaden) are fossorial. Most species of Hylidae, so the next available family-group ñame for the
Limnodynastes inhabit marshes; Taudacty/us lives along other genera formerly placed in the Cycloraninae is Lim-
mountain streams, and the aquatic Rheobatrachus lives nodynastinae. Heyer and S. Liem (1976) placed Rheo-
in mountain streams (Fig. 19-34). batrachus in its own subfamily, the Rheobatrachinae.
EVOLUTION
526

Figure 19-35. Distribution of living

members of the family
Myobatrachidae in Australia and
New Guinea and of the family
Leptodactylidae in the New World.

Laurent (1979) elevated this subfamily to the family level. 5. Limnodynastes Fitzinger, 1843 (Wagleria Gi-
Heyer and S. Liem's (1976) view of subfamilial relation- rará, 1853; Platyplectrum Günther, 1863;
ships was rejected by Farris et al. (1982), whose re- Opisthodon Steindachner, 1867; Heliorana
analysis of Heyer and S. Liem's data set showed Rheo- Steindachner, 1867; Ranaster MaCleay,
batrachus to be the sister taxon of the Limnodynastinae. 1878); 12 species. Australia, Tasmania, and
However, on the basis of immunological evidence, southern New Guinea. Miocene and Pleis-
Daugherty and Maxson (1982) placed Rheobatrachus in tocene of South Australia.
the Myobatrachinae. These different placements of 6. Megistolotis Tyler, Martin, and Davies, 1979;
Rheobatrachus reveal how little really is known about the 1 species. Northwestern Australia. Tyler et
relationships within the Myobatrachidae. Furthermore, the al. (1979).
family possibly is paraphyletic. J. D. Lynch's (1973) 7. Mixophys Günther, 1864; 4 species. Eastern
morphological analysis showed that limnodynastines and Australia. Straughan (1968).
the Heleophrynidae were similar to the leptodactylids, 8. Neobatrachus Peters, 1863; 7 species.
whereas myobatrachines and the Sooglossidae were more Southern and western Australia. Tyler et al.
similar to ranids. Reviews of the literature and synony- (1984).
mies of the Australian myobatrachids were presented by 9. Notaden Günther, 1873; 3 species. Northern
Cogger et al (1983). and southeastern Australia.
Contení.—The 20 living genera containing 99 species 10. Philoría Spencer, 1901; 1 species. Mount Baw
are grouped into two subfamilies: Baw, Victoria, Australia.
MYOBATRACHINAE Schlegel, 1850
LIMNODYNASTINAE Lynch, 1971 11. Arenophryne Tyler, 1976; 1 species. Coast
1. Adelotus Ogilby, 1907 (Cryptoíis Günther, of southern Western Australia. Tyler et al.
1863); 1 species. Eastern Australia. Moore (1980).
(1961). 12. Assa Tyler, 1972; 1 species. Mountains of
2. Heleioporus Gray, 1841 (Perialia Gray, in central eastern Australia. Ingram et al. (1975).
Eyre, 1845; Philocryphus Fletcher, 1894); 6 13. Crírtia Tschudi, 1838 (Ranidella Girará, 1853;
species. Southwestern and southeastern Ptemophrynus Lutken, 1863; Camario/ius
Australia. A. Lee (1967). Peters, 1863; Australocrinia Heyer and Liem,
3. Kyarranus Moore, 1958; 3 species. Moun- 1976); 13 species. Australia (except central
tains of eastern Australia. Ingram and Cor- parí), Tasmania, and eastern New Guinea.
ben (1975). Pleistocene of South Australia. Heyer et al.
4. Lechriodus Boulenger, 1882 (Asterophrys (1982).
Doria, 1875; Batrachopsis Boulenger, 1882; 14. Geocrinía Blake, 1973; 5 species. South-
Phanerotis Boulenger, 1890); 4 species. western and southeastern Australia; Tas-
Eastern New Guinea, Aru Islands, and east- mania. Pleistocene of South Australia. Blake
ern Australia. Zweifel (1972b). (1973).
 Classificatíon
15. t/ndobarrachus Noble, 1930; 1 species. Fossíí history.—None. 527
Eocene of India. Life history.—Large, unpigmented eggs are attached
16. Myobatrachus Schlegel, 1850 (Chelydoba- to rocks in streams. The torrent-adapted tadpoles have
trachus Günther, 1859); 1 species. Western large mouths with 4 upper and 11-17 lower rows of
Australia. denticles.
17. Poracrinia Heyer and Liem, 1976; 1 species. Remarks.—J. D. Lynch (1973) considered these frogs
Southeastern Australia. Heyer and S. Liem to be related to the limnodynastine myobatrachids. Heyer
(1976). and S. Liem (1976) suggested that Heleophryne should
18. Pseudophryne Fitzinger, 1843 (Bufonella be placed in its own family.
Girará, 1853; Metacrinia Parker, 1940; Contení.—The single genus contains three species:
Kankanophryne Heyer and Liem, 1976); 10
species. Eastern and western Australia; Tas- 1. Heleophryne Sclater, 1898; 3 species. South
mania. África. Poynton (1964).
19. Rheobatrachus Liem, 1973; 2 species.
Mountains of Queensland, Australia. Tyler
(1983); Mahony et el. (1984).
20. Taudacty/us Straughan and Lee, 1966; 5
species. Mountains of Queensland, Aus-
tralia.
21. Uperoleia Gray, 1841 (Hypero/ia Cope, 1865;
Glauertia Loveridge, 1933); 18 species.
Australia, except central and Southeastern
part; southern New Guinea. Tyler et al.
(1981).

HELEOPHRYNIDAE Noble, 1931

Definition.—There are eight ectochordal presacral
vertebrae with cartilaginous intervertebral joints and a
persistent notochord. The neural arches are imbrícate,
and Presacrals I and II are fused; the atlantal cotyles of
Figure 19-36. Heleophryne purcelli from Natal, South África.
Presacral I are closely juxtaposed. Ribs are absent. The Photo by J. Visser.
sacrum has rounded diapophyses and has a bicondylar
articulation with the coccyx, which has transverso processes
proximally. The pectoral girdle is arciferal and has a car-
tilaginous omosternum and sternum; the anterior end of
the scapula is not overlain by the clavicle. Palatines are
present; a parahyoid is absent, and the cricoid ring is
complete. The maxillae and premaxillae are dentate. The
astragalus and calcaneum are fused only proximally and
distally; there are two tarsalia, and the phalangeal for-
mula is normal. The m. sartorius is disünct from the m.
semitendinosus, and the tendón of the latter inserts ven-
tral to the m. gracilis; the m. glutaeus magnus has an
accessory tendón, and the m. adductor magnus has an
accessory head. The pupil is vertically elliptical. Amplexus
is inguinal. Type IV Larvae have denticles but no beaks;
the spiracle is sinistral, and the trigeminal and facial gan-
glia are fused. The diploid chromosome complement is
26.
Heleophrynids are moderate-sized (35-65 mm snout-
vent length) frogs that inhabit rocks in cascading moun-
tain streams (Fig. 19-36). The tadpoles are unique in
having large mouths lacking beaks.
Distribution.—The family is resrricted to the highlands
Figure 19-37. Distribution of living members of the family
and áreas of swiftly flowing streams in South África (Fig. Heleophrynidae in South África and of tne family Sooglossidae on
19-37). the Seychelles Islands.
EVOLUTION
538 SOOGLOSSIDAE Noble, 1931 unknown. Griffiths (1959a) proposed that these frogs
Deflnition.—There are eight presacral vertebrae with should be regarded as a subfamily of ranids. J. D. Lynch
a persisten! notochord and free intervertebral bodies in (1973) considered them to be a sister group of the myo-
subadults; in adults the intercentral bodies are fused to batrachines, a posiüon supported by Nussbaum's (1979b)
give procoelous centra. The neural arches are not im- interpretation of the karyotype and the amplectic position
brícate, and Presacrals I and II are not fused; the atlantal (Nussbaum, 1980).
cotyles of Presacral I are widely separated. Ribs are ab- Contení.—The three species are arranged in two gen-
sent. The sacrum has dilated diapophyses and a mono- era:
condylar artículatíon with the coccyx, which has small
transverse processes proximally. The pectoral girdle is 1. Nesomantis Boulenger, 1909; 1 species. Mahé
arciferal, but the epicoracoid cartilages are fused at their and Silhouette islands, Seychelles.
extreme anterior and posterior ends. A cartilaginous 2. Sooglossus Boulenger, 1906; 2 species. Mahé
omosternum and bony sternum are present; the scapula and Silhouette islands, Seychelles.
is not overlain anteriorly by the clavicle. Palatines are
present; a parahyoid is absent, and the cricoid ring is LEPTODACTYLIDAE Werner, 1896
incomplete ventrally. The maxillae and premaxillae are Deflnition.—There are eight presacral vertebrae with
dentate. The astragalus and calcaneum are fused only holochordal (stegochordal in some telmatobiines), pro-
proximally and distally; there are two tarsalia, and the coelous centra. The neural arches are imbrícate in cera-
phalangeal formula is normal. The m. sartorius is discrete tophryines and some telmatobiines and leptodactylines,
from the m. semitendinosus, and the tendón of the latter and nonimbricate in hylodines, some telmatobiines, and
passes dorsal to the m. gracilis; the m. glutaeus magnus most leptodactylines. Presacrals I and II are not fused
has an accessory tendón, and the m. adductor magnus (except in Telmatobufo); the atlantal cotyles of Presacral
has no accessory head. The pupil is horizontal. Amplexus I are closely juxtaposed ¡n ceratophryines and some tel-
is inguinal. Development is direct, or nonfeeding tadpoles matobiines, and widely separated in hylodines, leptodac-
lacking mouthparts and spiracles develop on the back of tylines, and other telmatobiines. Ribs are absent. The
the adult. The diploid chromosome complement is 26. sacrum has rounded diapophyses (weakly dilated in cer-
These small (snout-vent length to 40 mm) terrestrial atophrynines and some telmatobiines) and has a bicon-
frogs have the digits terminating in small, pointed discs dylar artículaüon with the coccyx, which lacks transverse
(Fig. 19-38). processes proximally (except in some telmatobiines). The
Distribution.—Sooglossids are restricted to the Sey- pectoral girdle is arciferal (pseudofirmisternal in ¡nsue-
chelles islands in the Indian Ocean (Fig. 19-37). tophrynus, SminthiHus, and Phrynopus peruvianas). A
Fossil history.—None. cartilaginous omosternum (absent in Lepidobatrachus,
Life history.—The eggs are terrestrial; those of Soo- Macrogenioglottus, Odontophrynus, Proceratophrys, and
g/ossus gardineri undergo direct development, whereas some Eleutherodactylus) and cartilaginous sternum are
the eggs of S. seychellensis hatch as nonfeeding tadpoles present (also bony postzonal elements in leptodacty-
that are carried on the back of the adult. These tadpoles lines). The anterior end of the scapula is not overlain by
lack a spiracle, internal gills, and mouthparts. the clavicle. Palatines are present; a parahyoid is absent,
Remarks.—The relatíonships of the sooglossids are and the cricoid ring is complete. The maxillae and pre-
maxillae are dentate (edentate in Batrachophn/nus, Lyn-
chophrys, SminthiHus, and some Physalaemus and Tel-
matobius). The astragalus and calcaneum are fused only
proximally and distally (completely fused in Geobatra-
chus); there are two tarsalia, and the phalangeal formula
is normal (reduced in Euparkerella and Phylhnastes).
The m. sartorius is distínct from the m. semitendinosus,
and the tendón of the latter is ventral to the m. gracilis
(penetrating m. gracilis in Crossodactylus and in some
Physalaemus); the m. glutaeus magnus has an accessory
tendón, and the m. adductor magnus has an accessory
head. The pupil is horizontal in most genera (vertícally
ellipücal in Caudiverbera, Hydrolaetare, Hylorina, Lepi-
dobatrachus, Limnomedusa, and Telmatobufo). Am-
plexus is axillary (inguinal in Batrachyla and some Pleu-
rodema). Aquatic Type IV larvae have denudes and beaks
(except Lepidobatrachus); the spiracle is sinistral (paired,
Figure 19-38. Nesomantis thomasseti from Mahé, Seychelles ventrolateral in Lepidobatrachus). The trigeminal and
Islands. Photo by E. D. Brodie, Jr. facial ganglia are fused. The diploid chromosome com-
 Classification
529

Figure 19-39. A. Ceratophrys

calcarata from South America.
B. Caudiuerbera caudiverbera from
Provincia Valdivia, Chile.
C. Eleutherodactyius latidiscus from
Departamento Valle, Colombia.
D. Hylorina sylvatica from Provincia
Llanquihue, Chile. E. Leptodactylus
chaquensis from Provincia Jujuy.
Argentina. F. Megaelosia goeldi from
Terezópolis, Brazil. A by K. T.
Nemuras; B-E by W. E. Duellman;
F. by J. P. Bogart.

plement varíes from 18 to 36; in addiüon, some Cera- era in México barely enter southwestern United States,
tophrys, Odontophrynus, and Pleurodema are poly- and two species of Eleutherodactylus have been intro-
ploids. duced into Florida.
Leptodactylids are extremely variable in size (12-250 Fossil histoty.—The family has an extensive fossil his-
mm) and diverse in structure and appearance. Some are tory throughout the Cenozoic in South America, where
toadlike (Odontophrynus); some are large-headed car- two genera are known only as fossils. Two living genera
nivores (Ceratophrys and Lepidobatrachus), and some are known from Pleistocene deposits in North America
are strictly aquatic (Batrachophrynus and Telmatobius and one from the West Indies.
(Fig. 19-39). Life history.—Primitive telmatobiines have aquatic eggs
Distribution.—Leptodactylids occur throughout most and tadpoles; leptodactylines have foam nests and aquatic
of South America, southern North America, and the West tadpoles, but the tadpoles complete their development
Indies (Fig. 19-35). Major centers of generic distribution in terrestrial nests in Adenomera. Others have terrestrial
are in the températe forests of Chile and the southern eggs that hatch into tadpoles that move to water (Tho-
Andes, highlands of southeastern Brazil, and the Pata- ropa) or hatch as advanced tadpoles that complete their
gonian-Chacoan región; secondary centers are in the development in the nest (Crossodactylodes, Cyc/oram-
northern Andes, Amazon Basin, and México. Three gen- phus, and Zachaenus). The species in at least nine gen-
EVOLUTION
"I era> of which Eleutherodactylus is the most numerous tral forests of Chile. Upper Oligocene to up-
and widespread, have direct development of terrestrial per Miocene of Patagonia; 1 fossil species
eggs. At least one species of Eleutherodactylus (¡aspen) from lower Eocene of Patagonia. J. D. Lynch
is viviparous and at least two (£. caqui and E. jasperi) (1978).
have internal fertilizaüon. 11. Crossodacty/odes Cochran, 1938; 1 species.
Remarks.—The leptodactylids were reviewed by J. D. Southeastern Brazil. J. D. Lynch (1971).
Lynch (1971), who recognized four subfamilies. Heyer 12. Cyclorhamphus Tschudi, 1838 (Pithecopsis
(1975) provided an alternativo phylogenetic arrange- Günther, 1859; Grypiscus Cope, 1867; Ili-
ment, and J. D. Lynch (1978) reviewed the lower tel- odiscus Miranda-Ribeiro, 1920; Craspedog-
matobiines. Some workers accord the ceratophryines fa- lossa Müller, 1922; Niedenia Ahí, 1923); 22
milial status. Accounts and colored illustrations of Chilean species. Southeastern Brazil. Heyer (1983).
and Argentine leptodactylids were provided by Cei (1962, 13. Dischidodactylus Lynch, 1979; 1 species.
1980). Cerro Duida, southern Venezuela. J. D.
Contení.—The 51 living and 2 fossil genera containing Lynch (1979b).
710 living species are grouped into four subfamilies: 14. Eleutherodactylus Duméril and Bibron, 1841
(Cornu/er Tschudi, 1838; Hylodes Fitzinger,
CERATOPHRYINAE Tschudi, 1838 1843; Euhyas Fitzinger, 1843; Craugastor
1. Ceratophrys Wied, 1824 (Stombus Graven- Cope, 1862; Strabomantis Peters, 1863;
horst, 1825; Phrynoceros Bibron, in Tschudi, Leiyla Keferstein, 1868; Limnophys Jimé-
1838; Trígonophrys Hallowell, 1856; Cha- nez de la Espada, 1870; Pristimantis Jimé-
cophrys Reig and Limeses, 1963); 6 species. nez de la Espada, 1870; Cyclocephalus Ji-
Discontinuous in tropical and subtropical ménez de la Espada, 1870; Hypodictyon
South America. Pliocene and Pleistocene of Cope, 1885; Basanitia Miranda-Ribeiro,
South America. J. D. Lynch (1982). 1923; Phrynanodus Ahí, 1933; Teletrema
2. Lepidobatrachus Budgett, 1899; 3 species. Miranda-Ribeiro, 1937; Microbatrachylus
Gran Chaco of Paraguay and Argentina. Cei Taylor, 1940; Ctenocranius Melin, 1941;
(1980). Pseudohyla Andersson, 1945; Amblyphry-
3. tWatue/ia Casamiquela, 1963; 1 species. Up- nus Cochran and Goin, 1961; Trachyphry-
per Miocene of Argentina. J. D. Lynch nus Cochran and Goin, 1963); 398 species.
(1971). México, Central America, and South Amer-
TELMATOBIINAE Fitzinger, 1843 ica southward to northern Argentina and
4. Adehphryne Hoogmoed and Lescure, 1984; Southeastern Brazil; West Indies; introduced
2 species. Guiana Shield in northeastern into Florida. Pleistocene of West Indies. J.
South America. Hoogmoed and Lescure D. Lynch (1976); A. Schwartz and Thomas
(1984). (1975).
5. Alsodes Bell, 1843 (Hammatodactylus Fitzin- 15. Euparkerelh Griffiths, 1959; 1 species.
ger, 1843; Cacoíus Günther, 1868); 10 spe- Southeastern Brazil. Heyer (1977).
cies. Austral forests of southern Argentina 16. Eupsophus Fitzinger, 1843 (Borborocoetes
and Chile. J. D. Lynch (1978). Bell, 1843); 5 species. Austral forests of
6. Atelognathus Lynch, 1978; 7 species. Pata- southern Argentina and Chile. Lower Oli-
gonian Argentina and Isla Wellington, Chile. gocene of Patagonia. J. D. Lynch (1978);
J. D. Lynch (1978). Formas and Vera (1982).
7. Barychohs Heyer, 1969; 2 species. Pacific 17. Geobatrachus Ruthven, 1915; 1 species. Sierra
lowlands of Ecuador; central Brazil. J. D. Nevada de Santa Marta, northern Colom-
Lynch (1980). bia. Ardila-Robayo (1979).
8. Batrachophrynus Peters, 1873; 1 species. 18. Holoaden Miranda-Ribeiro, 1920; 2 species.
Andean lakes in central Perú. J. D. Lynch Southeastern Brazil. J. D. Lynch (1971).
(1978). 19. Hylactophryne Lynch, 1968; 3 species. México
9. Batrachyla Bell, 1843; 3 species. Austral for- and southwestern United States. Pleistocene
ests of southern Argentina and Chile. J. D. of Texas. J. D. Lynch (1971).
Lynch (1978). 20. Hylorína Bell, 1843; 1 species. Austral forests
10. Caudiverbem Laurenti, 1768 (Calytocephal- of Chile. J. D. Lynch (1978).
ella Strand, 1828; Crossurus Wagler, 1830; 21. Insuetophrynus Barrio, 1970; 1 species. Aus-
Peltocephalus Bibron, in Tschudi, 1838; tral forests of Chile. J. D. Lynch (1978).
Calyptocephalus Duméril and Bibron, 1841; 22. Ischnocnema Reinhardt and Lütken, 1862
tEophractus Schaeffer, 1949; tGigantoba- (Oreobates Jiménez de la Espada, 1872); 3
trachus Casamiquela, 1959); 1 species. Aus- species. Western Amazon Basin, eastern
 Classificaüon
slopes of Andes, and southeastern Brazil. J. 1830; E/osia Tschudi, 1838; Scinacodes Fit- 531
D. Lynch (1971). zinger, 1843); 13 species. Southeastern Bra-
23. Lynchophrys Laurent, 1984; 1 species. Andes zil. Heyer (1982).
of central Perú. 42. Megaelosia Miranda-Ribeiro, 1923; 1 species.
24. Macrogenioglottus Carvalho, 1946; 1 spe- Southeastern Brazil. J. D. Lynch (1971).
cies. Eastern Brazil. Reig (1972). LEPTODACTYLINAE Werner, 1896
25. tNeoprocoe/a Schaeffer, 1949; 1 species. 43. Adenomera Steindachner, 1867; 6 species.
Lower Oligocene of Patagonia. J. D. Lynch Cis-Andean tropical South America. Heyer
(1971). (1974a).
26. Odontophrynus Reinhardt and Lütken, 1862 44. Edalorhina Jiménez de la Espada, 1870 (Bu-
(Hyperoodon Philippi, 1902); 5 species. bonius Cope, 1874); 2 species. Western
Eastern Brazil to northern Argentina, south- Amazon Basin. J. D. Lynch (1971).
ern Bolivia and Paraguay. Cei et al. (1982). 45. Hydrolaetare Gallardo, 1963; 1 species. Am-
27. Phrynopus Peters, 1874 (Noblella Barbour, azon Basin. J. D. Lynch (1971).
1930; Nicefororita Goin and Cochran, 1963); 46. Lepíodacty/us Fitzinger, 1826 (Cystignaíhus
16 species. Andes from Colombia to Bolivia. Wagler, 1830; Gnathophysa Fitzinger, 1843;
Cannatella (1984). Sibi/aírix Fitzinger, 1843; P/ectromantis Pe-
28. Phyí/onastes Heyer, 1977; 2 species. Upper ters, 1862; Eníomog/ossus Peters, 1870;
Amazon Basin. Heyer (1977). Pachypus Lutz, 1930; Carneóla Lutz, 1930;
29. Phyze/aphryne Heyer, 1977; 1 species. Am- Párvulas Lutz, 1930); 50 species. Tropical
azon Basin in Brazil. Hoogmoed and Les- and subtropical America from southern Texas
cure (1984). to central Argentina; Lesser Antilles and His-
30. Proceratophrys Miranda-Ribeiro, 1920; 10 paniola. Pleistocene of South America. Heyer
species. Coastal Brazil to northern Argen- (1970, 1978, 1979b).
tina. J. D. Lynch (1971). 47. Limnomedusa Fitzinger, 1843 (Litopleura Ji-
31. Scythrophrys Lynch, 1971; 1 species. South- ménez de la Espada, 1875); 1 species.
eastern Brazil. J. D. Lynch (1971). Southern Brazil, northern Argentina, Uru-
32. Sminíhií/us Barbour and Noble, 1920; 1 spe- guay. J. D. Lynch (1971).
cies. Cuba. J. D. Lynch (1971). 48. Lithodytes Fitzinger, 1843; 1 species. Ama-
33. Somuncuria Lynch, 1978; 1 species. Pata- zon Basin and Guianan región of South
gonian Argentina. J. D. Lynch (1978). America. J. D. Lynch (1971).
34. Syrrhophus Cope, 1878 (Epir/iexis Cope, 49. Parate/maíobius Lutz and Carvalho, 1958; 2
1866; Ma/achy/odes Cope, 1879); 15 spe- species. Southeastern Brazil. J. D. Lynch
cies. Texas to Guatemala and Belize. Pleis- (1971).
tocene of Texas. J. D. Lynch (1970). 50. Physa/aemus Fitzinger, 1826 (Pa/udico/a
35. Telmatobius Wiegmann, 1835 (Pseudobatra- Wagler, 1830; Liupurus Cope, 1860; Gom-
chus Peters, 1873; Cophaeus Cope, 1889); phobafes Reinhardt and Lütken, 1862; Eu-
29 species. Andes from Ecuador to central pemphix Steindachner, 1863; Nattereria
Argentina and Chile. J. D. Lynch (1978). Steindachner, 1864; ¡Hobates Fitzinger, in
36. Telmatobufo Schmidt, 1952; 3 species. South- Steindachner, 1867; Engystomops Jiménez
central Chile. Formas and Veloso (1982). de la Espada, 1872; Microphryne Peters,
37. Thoropa Cope, 1865; 3 species. Southeast- 1873; Pera/almos Jiménez de la Espada,
ern Brazil. Bokermann (1965b). 1875); 34 species. Tropical lowlands from
38. Tomodacty/us Günther, 1901; 9 species. México to Argentina. Cannatella and Duell-
Western and southern México. J. D. Lynch man (1984).
(1971). 51. Pleurodema Tschudi, 1838 (Chionope/as
39. Zachaenus Cope, 1866 (Oocormus Boulen- Tschudi, 1838; Leiuperus Duméril and Bi-
ger, 1905); 3 species. Southeastern Brazil. bron, 1841; Physa/aemus Fitzinger, 1843;
J. D. Lynch (1971). PMetaeus Girard, 1853; Lystris Cope, 1868);
HYLODINAE Günther, 1859 12 species. Discontinuous from Panamá to
40. Crossodacty/us Duméril and Bibron, 1841 extreme southern Argentina and Chile.
(Limnocharis Bell, in Darwin, 1843; Tarsop- Duellman and Veloso (1977).
terus Reinhardt and Lütken, 1862; Cala- 52. Pseudopa/udico/a Miranda-Ribeiro, 1926; 5
rnobates DeWitte, 1930); 5 species. South- species. Cis-Andean tropical South America.
eastern Brazil and northeastern Argentina. J. J. D. Lynch (1971).
D. Lynch (1971). 53. \7anzoiinius Heyer, 1974; 1 species. Upper
41. Hy/odes Fitzinger, 1826 (Enydrobius Wagler, Amazon Basin. Heyer (1974b).
EVOLUTION
533 BUFONIDAE Gray, 1825 (reduced in Crepidophryne, Didynamipus, Osorno-
Definition.—There are 5-8 holochordal, procoelous phryne, Pelophryne, and some Atelopus). The m. sar-
presacral vertebrae with imbrícate neural arches (inter- torius is discrete from the m. semitendinosus, and the
vertebral bodies not ossified in Pseudobufo). Variatíon in tendón of the latter passes ventral to the m. gracilis; the
the number of presacral vertebrae is the result of the m. glutaeus magnus has an accessory tendón, and the
fusión of Preseacrals I and II (e.g., Atelopus, Lepto- m. adductor magnus has an accessory head. The pupil
phryne, Oreophrynella, and Pelophryne). The atlantal is horizontal. Amplexus is axillary (secondarily inguinal
cotyles of Presacral I are juxtaposed. Ribs are absent. and dorsal in Osornophryne; inguinal and ventral in Nec-
The sacrum has dilated diapophyses and a bicondylar tophrynoides malcolmi and N. occidenta/is). Aquaüc Type
articulation with the coccyx, except in those taxa in which IV tadpoles have beaks and denudes; the spiracle is sin-
there has been a forward shift of the sacral articulation; istral, and the trigémina! and facial ganglia are fused. The
in these cases the original sacral vertebra is incorporated diploid chromosome complement is 22 (except 20 in the
into the coccyx, and there is a monocondylar articulation Bufo regularis complex).
or a fusión of the coccyx and the functíonal sacral ver- Toads and their allies generally have thick, glandular
tebra (e.g., (Didynamipus, Laurentophryne, Mertenso- skin with or without pustular warts; Bufo and some other
phryne, Nectophryne, Pelophryne, Wolterstorffina, and genera have parotoid glands, and some species have large
some/?/iamphophryne). Transverse processes are absent glands on the limbs (Fig. 19-40). Most species are ter-
on the coccyx. The pectoral girdle is arciferal or pseu- restrial or fossorial and have short limbs; the digits are
dofirmisternal by fusión of the epicoracoids (e.g., Atelo- reduced and shortened with a thick interdigital pad in
pus and Osornophryne). The omosternum is absent Osornophryne. Bufonids vary in size from the minute
(preseiit in Nectophrynoides, Wernería, and some Bufo], Oreophrynella (20 mm) to the gigantíc toad Bufo blom-
and a bony sternum is present; the scapula is not overlain bergi (250 mm). Most bufonids have extensively ossified
anteriorly by the clavicle. Palatínes are present (absent in skulls, and in most of these the skin is co-ossified with
Nectophryne and Pelophryne); a parahyoid is absent, the skull. The quadratojugals are reduced or lost in An-
and the cricoid ring is complete. The maxillae and pre- sonia, Laurentophryne, Nectophryne, Pelophryne, and
maxillae are edentate. The astragalus and calcaneum are Wolterstorffina; palatines are absent in some Dendro-
fused only proximally and distally; there are two tarsalia, phryniscus and JVfe/anophryniscus, and the columella is
and the phalangeal formula is normal in most genera absent in many genera and in some species of Atelopus,

Figure 19-40. A. Bufo blombergi

from Departamento Valle, Colombia
(photo by W. E. Duellman).
B. Atelopus varíus from Provincia
Veraguas, Panamá (photo by K.
Nemuras). C. Oreophrynella sp. from
Cerro Kukenan, Venezuela (photo by
R. W. McDiarmid).
D. Nectophrynoides osgoodi from
Balé Province, Ethiopia (photo
courtesy of the British Museum).
 Classificatíon
533

Figure 19-41. Distribution of living

members of the family Bufonidae.

Bu/o, and Nectophrynoides. The presence of a Bidder's Phylogenetic relaüonships among South American gen-
organ is unique to the bufonids (absent in some Den- era were discussed by McDiarmid (1971) and Trueb
drophryniscus); this is a paedomorphic feature—the re- (1971), and among African genera by Grandison (1978,
tentíon of a rudimentary ovary on the anterior end of the 1981).
testis (Fig. 14-23). Contení.—Twenty-five genera contain 335 living and
Distribution.—The family is cosmopolitan in tempér- 20 extinct species:
ate and tropical regions, except for the Australo-Papuan,
Madagascan, and Oceanic regions (Fig. 19-41). Bufo 1. Ansonia Stoliczka, 1870; 17 species. South-
marinus has been introduced into Australia, and New ern India, Malay Península, Tioman island,
Guinea and many other islands. Borneo, and Mindanao, Philippines. Inger
Fossil history.—The genus Bu/o is known from the (1960b).
upper Paleocene of South America and from upper Ter- 2. Atelopus Duméril and Bibron, 1841 (Phryn-
tiary and Quaternary deposits of North America, South idium Lichtenstein and Martens, 1856; Hy-
America, Europe, and África. laemorphus Schmidt, 1857; Phiríx Schmidt,
Life history.—Most bufonids deposit strings of nu- 1857); 43 species. Costa Rica to Solivia;
merous small, pigmented eggs in water where general- Guianan región and coastal eastern Brazil.
ized pond-type tadpoles develop. Peculiar crownlike 3. Bu/o Laurentí, 1768; (Batrachus Rafinesque,
structures are present on the head of tadpoles of Mer- 1814; Bu/otes Rafinesque, 1815; Oxyrhyn-
tensophryne and Stephopaedes (Fig. 6-17F). The tad- chus Spix, 1824; Chascax Oken, 1828;
poles of Ansonía and Atelopus develop in torrential streams ChaunusWagler, 1828; Otilopha Gray, 1831;
and have large oral discs (Figs. 6-15C, 6-16C). Oreo- Phryniscus Wiegmann, 1834; tPa/aeophry-
phrynella, Osornophryne, Pelophryne, Rhampho- nos Tschudi, 1838; Sclerophrys Bibron, in
phryne, and some Atelopus have large, unpigmented eggs. Tschudi, 1838; Osilophus Cuvier, in Tschudi,
Pehphryne has an abbreviated tadpole stage that sur- 1838; Chihphiyne Fitzinger, 1843; ¡ncilius
vives on yolk; the same may be true for other bufonids Fitzinger, 1843; Docidophryne Fitzinger,
with large, unpigmented eggs, or possibly they undergo 1843; Eurhina Fitzinger, 1843; Phrynoidis
direct development. Some species of Nectophrynoides Fitzinger, 1843; Phrynomorphus Fitzinger,
produce tadpoles; others are ovoviviparous or vivipa- 1843; Phryne Oken, 1843; Anaxyrus
rous. Fertilizatíon is internal in some Nectophrynoides Tschudi, 1845; Trachycara Tschudi, 1845;
and in Mertensophryne micmnotis. Adenomus Cope, 1860; Rhaebo Cope,
Remarks.—Some of the genera that are now con- 1862; Epidalea Cope, 1865; Pegaeus Gistel,
tained in the Bufonidae formerly were placed in the Ate- 1868; Nannophryne Günther, 1870; Cran-
lopodidae. On the basis of the presence of a Bidder's opsis Cope, 1876; Ollotis Cope, 1876; tP/a-
organ all of the genera were placed in the Bufonidae, tosphus L'Isle, 1877; Dromolectrus Cam-
except Bmchycephalus (Bidder's organ absent), which is erano, 1879; tBu/auus Portís, 1885;
now placed in the Brachycephalidae (McDiarmid, 1971). Cranophryne Cope, 1889; Ancudia Phi-
Toads of the genus Bufo were reviewed by W. Blair (1972). lippe, 1902; Aruncus Philippi, 1902; Steno-
EVOLUTION
534 dactylus Philippi, 1902); 205 species. Cos- 19. Peltophryne Fitzinger, 1843 (Otaspis Cope,
mopolitan except for Arctic regions, New 1868); 8 species. Greater Antilles. Pregill
Guinea, Australia, New Zealand, and South (1981).
Pacific islands; Bufo marinos introduced in 20. Pseudobufo Tschudi, 1838 (Py/eus Gistel,
Australia, New Guinea, and on many trop- 1848; Ñecles Cope, 1865); 1 species. Malay
ical islands. Numerous Recent and extinct Península, Sumatra, Borneo. Inger (1966).
species known as fossils from the Paleocene, 21. Rhamphophryne Trueb, 1971; 6 species.
Miocene, Pliocene, and Pleistocene of South Mountains from western Panamá to Ecua-
America, lower Miocene through Pleisto- dor; northeastern Brazil. Trueb (1971).
cene of North America, upper Oligocene 22. Schismaderma Smith, 1849; 1 species. Tan-
through Pleistocene of Europe, and Pli- zania and Zaire to South África. Poynton
ocene of North África. W. Blair (1972). (1964).
4. Bufoides Pillai and Yazdani, 1973; 1 species. 23. Stephopaedes Channing, 1978; 1 species.
Assam, India. Southern Tanzania, western Mosambique,
5. Capensibufo Grandison, 1980; 2 species. and Zimbabwe. Channing (1978).
Mountains of Cape Province, South África. 24. Werneria Posch, 1903 (Stenog/ossa Anders-
Grandison (1980a). son, 1903); 4 species. Togo and Cameroon,
6. Crepidophryne Cope, 1889 (Crepidius Cope, West África. Amiet (1976).
1876); 1 species. Mountains of western Pan- 25. Wolterstürffina Mertens, 1939; 2 species.
amá and adjacent Costa Rica. J. Savage and Western África in Nigeria and Cameroon.
Kluge (1961). Perret (1972).
7. Dendrophryniscus Jiménez de la Espada,
1871; 3 species. Atlantic forests of Brazil, BRACHYCEPHALIDAE Günther, 1859
Guianas, upper Amazon Basin. McDiarmid Deflnition.—There are seven holochordal, procoelous
(1971). presacral vertebrae with imbrícate neural arches. Presa-
8. Didynam/pus Andersson, 1903 (Atelophryne crals I and II are fused, and the atlantal cotyles of Pre-
Boulenger, 1905); 1 species. Cameroon and sacral I are widely separated. Ribs are absent. The sa-
Fernando Po island. Grandison (1981). crum has dilated diapophyses and a bicondylar artículation
9. Laurentophryne Tihen, 1960; 1 species. with the coccyx, which lacks transverse processes. The
Kiandjo, Zaire. Grandison (1981). pectoral girdle is arciferal, but the epicoracoids are com-
10. Leptophryne Fitzinger, 1843 (Cacophryne pletely ossified and articulating throughout most of their
Davis, 1935); 2 species. Malay Península and length. The omosternum and sternum are absent; the
Greater Sunda Islands. Dubois (1982). scapula is not overlain anteriorly by the clavicle. Palatines
11. Melanophryniscus Gallardo, 1961; 8 species. and prevomers are absent; a parahyoid is absent, and
Southern Brazil, Uruguay, Paraguay, and the cricoid ring is complete. The maxillae and premaxillae
northern Argentina. McDiarmid (1971). are edentate. The astragalus and calcaneum are fused
12. Mertensophryne Tihen, 1960; 2 species. only proximally and distally; there are two tarsalia, and
Central África from Zaire eastward to Zan- the phalangeal formula is greatly reduced—1-2-3-1 and
zíbar. Grandison (1981). 0/1-2-3-4-1. The m. sartorius is distínct from the m. semi-
13. Nectophryne Buchholz and Peters, 1875; 2 tendinosus, and the tendón of the latter inserts ventral to
species. Western África from Nigeria to Zaire; the m. gracilis; the m. glutaeus magnus has an accessory
Fernando Po island. tendón, and the m. adductor magnus has an accessory
14. Nectophrynoides Noble, 1926; 8 species. head. The pupil is horizontal. Amplexus is axillary. Aquatic
Mountains of Central África in Liberta, tadpoles presumably are absent. The diploid chromo-
Guinea, Ethiopia, and Tanzania. Grandison some complement is 22.
(1978, 1981). Brachycephalids have body lengths of less than 16 mm
15. Oreophrynella Boulenger, 1895; 2 species. and greatly reduced phalanges (Fig. 19-42); there are
Mountains of Guyana and southern Vene- only two functional digits on the hand and three on the
zuela. McDiarmid (1971). foot. A dermal bony shield ossifies dorsal to the vertebrae
16. Osornophryne Ruíz and Hernández, 1976; 2 in Brachycephalus (Fig. 14-5).
species. Andes of Colombia and northern Distribution.—The family is restricted to the humid
Ecuador. Ruíz and Hernández (1976). coastal región of southeastern Brazil (Fig. 19-43).
17. Pedostibes Günther, 1875; 6 species. South- Fossil history.—No fossils are known.
ern India; Malay Península to Sumatra and Life history.—The presence of few, large, unpig-
Borneo. Inger (1966). mented ovarían eggs is indicatíve of direct development
18. Pelophryne Barbour, 1938; 8 species. Ma- of terrestrial eggs.
laya, Hainan island (China), Borneo, and Remarks.—Izecksohn (1971) described skeletal vari-
the Philippines. Inger (1960a). ation in Brachycepha/us, and McDiarmid (1971) noted
 Classification
535

Figure 19-42. Brachycephalus ephippium from Brazil. Photo by

J. P. Bogart.

the absence of a Bidder's organ in Brachycephalus and

removed the genus from the Bufonidae.
Contení.—Two monotypic genera are recognized:

1. Brachycephalus Fitzinger, 1826 (Ephippipher

Cocteau, 1835); 1 species. Eastern and
southeastern Brazil. Cochran (1955).
2. Psyllophryne Izecksohn, 1971; 1 species. For-
ests in state of Rio de Janeiro, Brazil. Izeck-
sohn (1971).
Figure 19-43. Distribution of living members of the family
Brachycephalidae and of the family Rhinodermatidae in South
RHINODERMATIDAE Bonaparte, 1850 America.
Definition.—There are eight, holochordal, procoelous
presacral vertebrae with imbrícate neural arches. Presa-
crals I and II are fused, and the atlantal cotyles of Pre- Fossil history.—No fossils are known.
sacral I are juxtaposed. Ribs are absent. The sacrum has Life history.—Up to 40 large, unpigmented eggs are
broadly dilated diapophyses and a bicondylar articulation laid on land. Upon hatching, the tadpoles are picked up
with the coccyx, which lacks transverse processes. The by the males. Once in the buccal cavity, the tadpoles of
pectoral girdle is pseudofirmisternal (epicoracoids fused Rhinoderma rufum are carried to small pools of water
posterior to level of sternum); a cartílaginous omoster- where they complete their development. The nonfeeding
num and sternum are present, and the scapula is not tadpoles of í?. darwinii complete their development in
overlain anteriorly by the clavicle. Palatines are absent; the vocal sacs of males.
a parahyoid is absent, and the cricoid ring is complete. Remarks.—Rhinoderma is an enigmatíc genus placed
The maxillae and premaxillae are edentate. The astrag- by Noble (1931b) in his heterogeneous Brachycephali-
alus and calcaneum are fused only proximally and dis- dae. Griffiths (1959b) placed Rhinoderma in the Lepto-
tally; there are three tarsalia, and the phalangeal formula dactylidae, and J. D. Lynch (1971) relegated it to its own
is normal. The m. sartorius is discrete from the m. semi- family.
tendinosus, and the tendón of the latter inserts ventral to Contení.—One genus contains two species;
the m. gracilis; the m. glutaeus magnus has a long, slen-
der accessory tendón, and the m. adductor magnus lacks 1. Rhinoderma Duméril and Bibron, 1841
an accessory head. The pupil is horizontal. Amplexus is (Heminectes Philippi, 1902); 2 species. Hu-
axillary. Type IV tadpoles have beaks and denticles; the mid austral forests of Argentina and Chile.
spiracle is sinistral. The diploid chromosome complement Formas et al. (1975).
is26.
Rhinodermaüds are small (30 mm) and have a fleshy PSEUDIDAE Fitzinger, 1843
proboscis (Fig. 19-44); the skull is weakly ossified. Definition.—There are eight, holochordal, procoelous
Distribution.—This family is restricted to températe presacral vertebras with nonimbricate neural arches. Pre-
forests in southern Chile and Argentina (Fig. 19-43). sacrals I and II are not fused, and the atlantal cotyles of
EVOLUTION
536 They have large, protuberant eyes, robust hindlimbs and
fully webbed feet (Fig. 19-45).
Distríbution.—Members of this family inhabit tropical
lowlands east of the Andes and also in the Magdalena
Valley (Colombia) in South America (Fig. 19-46).
Fossil history.—No fossils are known.
Life history.—Aquatic eggs develop into enormous
tadpoles (250 mm in Pseudis paradoxa) and transform
into relaüvely small frogs.
Remarks.—Prior to the resurrection of the Pseudidae
by J. Savage and Carvalho (1953), these frogs were placed
in the Hylidae or Leptodactylidae.
Contení.—Four species are recognized in two genera:

Figure 19-44. Rhinoderma darwinii from Provincia Malleco, 1. Lysapsus Cope, 1862 (Podonectes Fitzinger,
Chile. Photo by W. E. Duellman. 1864); 2 species. Tropical South America east
of the Andes. Duellman (1977).
2. Pseudis Wagler, 1830 (Batmchychthys Pizarra,
1876); 2 species. Tropical South America east
of the Andes. Gallardo (1961).

HYLIDAE Gray, 1825

Definition.—There are eight holochordal, procoelous
presacral vertebrae with nonimbricate neural arches in
most taxa (imbrícate in phyllomedusines). Presacrals I

Figure 19-45. Pseudis paradoxa from Estado Sucre, Venezuela.

Photo by W. E. Duellman.

Presacral I are juxtaposed. Ribs are absent. The sacrum

has rounded diapophyses and a bicondylar articulation
with the coccyx, which lacks transverse processes. The
pectoral girdle is arciferal; a cartilaginous omosternum
and sternum are present, and the scapula is not overlain
anteriorly by the clavicle. Palatínes are present; a para-
hyoid is absent, and the cricoid ring is complete. The
maxillae and premaxillae are dentate. The astragalus and
calcaneum are fused only proximally and distally; there
are two tarsalia, and the phalangeal formula is increased
by the additíon of long, ossified intercalan/ elements be-
tween the terminal and penultimate phalanges. The m.
sartorius is discrete from the m. semitendinosus, and the
tendón of the latter passes ventral to the m. gracilis; the
m. glutaeus magnus has an accessory tendón, and the
m. adductor magnus has an accessory head. The pupil
is horizontal. Amplexus is axillary. All have aquatic Type
IV tadpoles with beaks and denudes; the spiracle is sin-
istral, and the trigémina! and facial ganglia are fused. The
diploid chromosome complement is 24. Figure 19-46. Distribution of living members of the family
These aquatic frogs attain body lengths up to 70 mm. Pseudidae in South America.
 Classification
537

Figure 19-47. A. Litorio dahlii from

Northern Territory, Australia.
B. Phyllomedusa tarsius from Estado
Bolívar, Venezuela. C. Gastrotheca
testudínea from Provincia Ayacucho,
Perú. D. Hemiphractus bubalus from
Provincia Ñapo, Ecuador. E. Hyla
lindae from Provincia Ñapo,
Ecuador, f. Triprion petasatus from
Yucatán, México. Photos by W. E.
Duellman.

and II are not fused, and the atlantal cotyles of Presacral has no accessory tendón, and the m. adductor magnus
I are widely separated. Ribs are absent. The sacrum has has an accessory head. The pupil is horizontal (vertically
dilated diapophyses (round in Acris and some neotropical ellipücal in phyllomedusines andNyctimysf.es). Amplexus
hylines) and has a bicondylar articulatíon with the coccyx, is axillary. Most have aquatic Type IV larvae with beaks
which lacks transverse processes. The pectoral girdle is and denudes (absent in some neotropical Hyla) and a
arciferal and has a cartilaginous omosternum (absent in sinistral spiracle varying in positíon from midlateral to
A/íophryne) and sternum; the scapula is not overlain an- nearly midventral; the trigeminal and facial ganglia are
teriorly by the clavicle. Palatines usually are present; a fused. Direct development of eggs carried by the female
parahyoid is absent, and the cricoid ring is complete. The is characteristic of most hemiphractines. The diploid
maxillae and premaxillae are dentate (edentate in A//o- chromosome complement is 22-30.
phryne). The astragalus and calcaneum are fused only Hylids are extremely variable in size (17-140 mm) and
proximally and distally; there are two tarsalia, and the external appearance, but distinctive toe pads usually are
phalangeal formula is increased by the addition of a short, present. Most hylids are arboreal, but some (Acris) are
cartilaginous intercalan/ element between the penulti- aquatic and others (Cyc/orana and Pternony/a) are fos-
mate and terminal phalanges (element cartilaginous, os- sorial (Fig. 19-47).
sified, or absent in Cyc/orana). The m. sartorius is discrete Distribución.—The family occurs throughout tempér-
from the m. semitendinosus, and the tendón of the latter ate North America, Central America, the West Indies, and
inserís ventral to the m. gracilis; the m. glutaeus magnus tropical South America; it also occurs throughout Aus-
EVOLUTION
538

Figure 19-48. Distribution of living

members of the family Hylidae.

tralia, Tasmania, New Guinea, and the Solomon Islands. A checklist containing all of the taxa named through 1974
The genus Hy/a also occurs throughout most of tempér- is available (Duellman, 1977).
ate Eurasia, Japan, and extreme northern África (Fig. 19- Contení.—Four subfamilies containing 630 species in
48). 37 living genera are recognized, in addition to 2 mono-
Fossil history.—Hylids are known from the Oligocene typic fossil genera:
through the Pleistocene in North America, from the Mio-
cene through the Pleistocene of Europe, and from the PELODRYADINAE Günther, 1859
Miocene and Pleistocene of Australia. Hylids also are 1. tAustra/obaírachus Tyler, 1976; 1 species.
known from the Paleocene of Brazil (Estes and Reig, Middle Miocene of South Australia. Tyler
1973). Two genera are known only as fossils. (1982).
Life history.—Hylines and pelodryadines normally have 2. Gyclorana Steindachner, 1867 (Chiroleptes
aquaüc eggs and tadpoles, but some species of Hy/a and Günther, 1859; Phractops Peters, 1867); 13
Litaría, and all phyllomedusines deposit eggs on vege- species. Australia. Tyler et al. (1978).
tation over ponds or streams, into which the hatching 3. Litaría Tschudi, 1838 (Ranoidea Tschudi,
tadpoles drop. Anotheca, Nyctimantis, and Phrynohyas 1838; Lepíhy/a Duméril and Bibron, 1841;
resinifictrix deposit their eggs in water-filled cavitíes in Euscelis Fitzinger, 1843; Pelobius Fitzinger,
trees. The eggs and tadpoles of some Hy/a develop in 1843; Polyphone Gistel, 1848; Pelodryas
bromeliads. Hemiphractines brood the eggs on the dor- Günther, 1859; Chirodryas Keferstein, 1867;
sum (Cryptobatrachus, Hemiphractus, and Stefania) or Fanchonia Werner, 1893; Mítro/ysís Cope,
in a dorsal brood pouch (other genera) of the females. 1889); 106 species. New Guinea, Moluccan
The developing embryos have large, external gills and Islands, Lesser Sunda Islands, Timor, Bis-
hatch as tadpoles in F/ecíonotus, Frite/ana, and some marck Archipelago, Solomon Islands, Aus-
Gastrotheca and as froglets in the other genera. tralia, and Tasmania; introduced into New
Remarks.—The relationships of the Australopapuan Caledonia and New Zealand. Miocene and
genera to the other hylids remains questíonable. Allo- Pliocene of Australia. Tyler and M. Davies
phryne is placed tentatively in the Hylidae (Duellman, (1978a).
1975). J. Savage (1973) placed Altophryne in its own 4. Nyctimystes Stejneger, 1916; 26 species. New
family, but because the family was not diagnosed, it has Guinea, eastern Moluccan Islands, and
no taxonomic validity. The Australopapuan genera were northern Queensland, Australia. Tyler and
reviewed by Tyler and M. Davies (1978a, 1979a), and M. Davies (1979a).
the Middle American species were monographed by PHYLLOMEDUSINAE Günther, 1859
Duellman (1970). Accounts of Colombian species are 5. Agalychnis Cope, 1864; 8 species. Southern
available in Cochran and Goin (1970). The Brazilian spe- México to Ecuador. Duellman (1977).
cies of Hy/a were treated by B. Lutz (1973); the West 6. Pachymedusa Duellman, 1968; 1 species.
Indian hylids were surveyed by Trueb and Tyler (1974), Pacific lowlands of México. Duellman (1970).
and the Argentinean species were treated by Cei (1980). 7. Phyllomedusa Wagler, 1830 (Pií/iecopus
 Classification
Cope, 1866; Hy/omantis Peters, 1872; 1799; Hy/aria Rafinesque, 1814; Boana 539
Phrynomedusa Miranda-Ribeiro, 1923; Gray, 1825; Hypsiboos Wagler, 1830; Au-
Bradymedusa Miranda-Ribeiro, 1923); 33 letrís Wagler, 1830; Hyas Wagler, 1830;
species. Tropical South America to Costa Scinox Wagler, 1830; Dendrohyas Wagler,
Rica. Duellman (1977). 1830; Lophopus Tschudi, 1838; Hypsipso-
HEMIPHRACTINAE Peters, 1862 phus Fitzinger, 1843; Lobipes Fitzinger, 1843;
8. Ampriignaí/iodon Boulenger, 1882; 1 spe- Phyllobius Fitzinger, 1843; Dendropsophus
cies. Andean slopes of Ecuador and south- Fitzinger, 1843; Dryophytes Fitzinger, 1843;
ern Colombia. Centrotelma Burmeister, 1856; Hy/ome-
9. Cryptobatrachus Ruthven, 1916; 3 species. dusa Burmeister, 1856; Hylella Reinhardt and
Andean slopes of central and northern Col- Lütken, 1862; Cinc/idium Cope, 1867; Cin-
ombia. cliscopus Cope, 1870; Cophomantis Peters,
10. Flectonotus Miranda-Ribeiro, 1926; 2 spe- 1870; Exerodonta Brocchi, 1879; Hy/ono-
cies. Northern Venezuela, Trinidad, and To- mus Peters, 1882; Hy/oscirtus Peters, 1882;
bago. Duellman and Gray (1983). Epedaphus Cope, 1885; Hy/ío/a Mocquard,
11. Fritziana Mello-Leitao, 1937 (Coelonotus Mi- 1899; Guentheña Miranda-Ribeiro, 1926);
randa-Ribeiro, 1920; Frítela Mello-Leitao, 251 species. North, Central, and South
1920; Nototheca Bokermann, 1950); 3 spe- America; Greater Antilles; Eurasia, except
cies. Mountains of southeastern Brazil. tropical southeastern Asia; África north of
Duellman and Gray (1983). Sahara. Oligocene through Pleistocene of
12. Gastrotheca Fitzinger, 1843 (Notodelphys North America; Miocene through Pleisto-
Lichtenstein and Weinland, 1854; Noto- cene of Europe. Duellman (1977).
trema Günther, 1859; Opisthodelphys 24. Limnaoedus Mittleman and List, 1953; 1 spe-
Günther, 1859); 37 species. Andean región cies. Southeastern United States. Franz and
of South America from Venezuela to north- Chantell (1978).
ern Argentina; eastern Brazil; Panamá. 25. Nyctimantis Boulenger, 1882; 1 species.
13. Hemiphractus Wagler, 1830 (Cerathyla Ji- Amazonian Ecuador. Duellman and Trueb
ménez de la Espada, 1871); 5 species. (1976).
Northwestern South America; Panamá. Trueb 26. O/o/ygon Fitzinger, 1843 (Garbearía Mi-
(1974). randa-Ribeiro, 1926); 54 species. Tropical
14. Stefania Rivero, 1968; 7 species. Guianan America from México to northern Argentina.
highlands, northeastern South America. Fouquette and Delahoussaye (1977).
Duellman and Hoogmoed (1984). 27. Osteocephalus Steindachner, 1862; 6 spe-
HYLINAE Gray, 1825 cies. Tropical South America east of the
15. Acris Duméril and Bibron, 1841; 2 species. Andes. Trueb and Duellman (1971).
Eastern North America. Lower Miocene 28. Osteopilus Fitzinger, 1843; 3 species. Greater
through Pleistocene of North America. Antilles, Bahamas, Florida. Trueb and Tyler
Duellman (1977). (1974).
16. Allophiyne Gaige, 1926; 1 species. Guianan 29. P/irynohyas Fitzinger, 1843 (Acrodytes Fit-
región of northeastern South America. zinger, 1843; Scytopis Cope, 1862); 5 spe-
Hoogmoed (1969). cies. Tropical America from México to
17. Anotheca Smith, 1939; 1 species. Southern northern Argentina. Duellman (1971).
México and Central America. Duellman 30. Phyí/odytes Wagler, 1830 (Amphodus Pe-
(1970). ters, 1872; Lophyohyla Miranda-Ribeiro,
18. Aparasphenodon Miranda-Ribeiro, 1920; 2 1923); 4 species. Eastern Brazil; Trinidad.
species. Coastal southeastern Brazil; upper Bokermann (1966a).
Orinoco Basin, Venezuela. Trueb (1970a). 31. P/ectroriy/a Brocchi, 1877 (Caupriias Broc-
19. Aplastodiscus Lutz, 1950; 1 species. Central chi, 1877); 13 species. Highlands of nuclear
and southeastern Brazil. Cochran (1955). Central America. Duellman and Campbell
20. Argenteohyla Trueb, 1970; 1 species. Río (1984).
Paraná and Delta La Plata, Argentina and 32. tProacris Holman, 1961; 1 species. Miocene
Uruguay. Trueb (1970b). of Florida. Holman (1968).
21. Calyptahyla Trueb and Tyler, 1974; 1 spe- 33. Pseudacris Fitzinger, 1843 (Chorophilus Baird,
cies. Jamaica. Trueb and Tyler (1974). 1854; Helocaetes Baird, 1854); 7 species.
22. Corythomantis Boulenger, 1896; 1 species. Eastern North America. Upper Miocene
Northeastern Brazil. Trueb (1970a). through the Pleistocene of North America.
23. Hyla Laurenti, 1768 (Calamita Schneider, Duellman (1977).
EVOLUTION
540

Figure 19-49. A. Centro/ene

geckoideum from Provincia
Pichincha, Ecuador. B. Centrolenella
prosoblepon from Provincia Alajuela,
Costa Rica. Photos by W. E.
Duellman.

34. Ptemohyla Boulenger, 1882; 2 species. is axillary. All have aquatic Type IV tadpoles with beaks
Western México; Atizona. Trueb (1969). and denudes; the spiracle is sinistral, and the trigeminal
35. Ptychohyla Taylor, 1944; 6 species. Southern and facial ganglia are fused. The chromosome comple-
México and northern Central America. ment is 20.
Duellman and Campbell (1982). Most centrolenids are small (30 mm) with transparent
36. Smilisca Cope, 1865; 6 species. Southern skin on the venter (Fig. 19-49); Centro/ene geckoideum
Texas to northwestern South America. is much larger (77 mm). The terminal phalanges are T-
Duellman (1970). shaped, and there is a medial protuberance on the third
37. Sphaenorhynchus Tschudi, 1838 (Dryome- metatarsal.
íictes Fitzinger, 1843; Hy/opsis Werner, 1894; Distríbution.—The family occurs in humid regions from
Sphoenohyla Lutz and Lutz, 1948); 11 spe- southern México to Bolivia and northeastern Argentina
cies. Tropical South America east of the (Fig. 19-50); the greatest diversity of species is on the
Andes. Duellman (1977). slopes of the Andes in northwestern South America and
38. Tmchycephalus Tschudi, 1838 (Tetraprion secondarily in Costa Rica and Panamá.
Stejneger and Test, 1891); 3 species. East- Fossil history.—No fossils are known.
ern Brazil; coastal northwestern South Life history.—Small clutches of eggs are deposited on
America. Trueb (1970a). leaves (Centro/ene/la) or rocks (Centro/ene) above streams
39. Triprion Cope, 1866 (Pharyngodon Cope, and may be attended by territorial males. Elongate tad-
1865; Diaglena Cope, 1887); 2 species. poles (Fig. 6-15F) develop in gravel or detritus in flowing
Western México and Yucatán Península. water.
Duellman (1970). Remarks.—Centrolenids are distinguished from hylids
by the presence of a fused astragalus and calcaneum, T-
CENTROLENIDAE Taylor, 1951 shaped terminal phalanges, and a median protuberance
Definition.—There are eight holochordal, procoelous on the third metacarpal.
presacral vertebrae with nonimbricate neural arches. Pre- Contení.—Two genera containing 65 species are rec-
sacrals I and II are not fused, and the atlantal cotyles of ognized:
Presacral I are widely separated. Ribs are absent. The
sacrum has dilated diapophyses and a bicondylar artic- 1. Centro/ene Jiménez de la Espada, 1872; 1
ulation with the coccyx, which lacks transverse processes. species. Andean slopes of Colombia and Ec-
The pectoral girdle is arciferal and has a sternum but no uador. J. D. Lynch et al. (1983).
omosternum; the scapula is not overlain anteriorly by the 2. Centrolenella Noble, 1920 (Cochranella Tay-
clavicle. Palatines are present; a parahyoid is absent, and lor, 1951; Teratohyla Taylor, 1951); 64 spe-
the cricoid ring is complete. The maxillae and premaxillae cies. Tropical America from México to Bolivia
are dentate. The astragalus and calcaneum are fused and northeastern Argentina. Duellman (1977).
throughout their lengths; there are two tarsalia, and the
phalangeal formula is increased by the addition of a short, DENDROBATIDAE Cope, 1865
carülaginous intercalary element between the penultí- Definition.—There are eight holochordal, procoelous
mate and terminal phalanges. The m. sartorius is discrete presacral vertebrae with nonimbricate neural arches. Pre-
from the m. semitendinosus, and the tendón of the latter sacrals I and II are not fused, but Presacral VIH is syn-
inserís ventral to the m. gracilis; the m. glutaeus magnus ostoücally united with the sacrum in some Dendrobates;
lacks an accessory tendón, and the m. adductor magnus the atlantal cotyles of Presacral I are widely separated.
has an accessory head. The pupil is horizontal. Amplexus Ribs are absent. The sacrum has rounded diapophyses
 Classification
and a bicondylar articulation with the coccyx, which usu- head. The pupil is horizontal. Amplexus is cephalic or 541
ally has transverse processes proximally. The pectoral absent in some species. Aquatic Type IV tadpoles have
girdle is firmistemal; a carülaginous omostemum and bony beaks and denudes; the spiracle is sinistral, and the tri-
sternum are present, and the scapula is not overlain an- geminal and facial ganglia are fused. The diploid chro-
teriorly by the clavicle. Palatines are present or absent; a mosome complement is 18-24.
parahyoid is absent, and the cricoid ring is complete. The Most dendrobatids are smaller than 50 mm. A pair of
maxillae and premaxillae are dentate or edentate. The scalelike scutes is present on the dorsal surface of each
astragalus and calcaneum are fused only proximally and terminal phalange (Fig. 19-51). Most known species of
distally; there are two tarsalia, and the phalangeal for- Dendrobates and Phyllobates are brightly colored and
mula is normal. The m. sartorius is discrete from the m. have toxic skin secretions. Atopophrynus and Coloste-
semitendinosus, and the tendón of the latter pierces the thus tend to be dully colored and most seem to lack toxic
m. gracilis; the m. glutaeus magnus has an accessory skin secretions.
tendón, and the m. adductor magnus has an accessory Distribution.—All genera occur in northwestem South
America. The distribution of the family extends in humid
tropical and subtropical regions from Nicaragua to south-
eastern Brazil and Solivia (Fig. 19-52).
Fossil history.—No fossils are known.
Life history.—Small clutches of unpigmented eggs are
deposited in humid terrestrial and arboreal situations. Either
males or females remain with, or periodically visit, the
nest and carry tadpoles on their backs to water, where
the tadpoles complete their development. Females of some
species of Dendrobates place individual tadpoles in water
in the axils of bromeliads and then periodically return to
the site of each tadpole and deposit unfertilized eggs,
which are eaten by the tadpoles.
Remarks.—Griffiths (1959b) considered dendrobatids
to be a subfamily of the Ranidae, whereas J. D. Lynch
(1973) posited that dendrobatids were related to elosiine
(= hylodine) leptodactylids. J. D. Lynch and Ruíz (1982)
discussed the generic classification. The generic alloca-
tions of species to Phyllobates and Dendrobates by Sil-
verstone (1975,1976) was modified by Myers et al. (1978),
who also summarized exisüng informatíon on skin secre-
tions and use of the skin toxins on poison darts.
Contení.—Four genera containing 117 species are
recognized:

1. Atopophrynus Lynch and Ruíz, 1982; 1 spe-

cies. Andes of northern Colombia. J. D. Lynch
Figure 19-50. Distribution of living members of the family and Ruíz (1982).
Centrolenidae. 2. Cohstethus Cope, 1866 (Prostherapis Cope,

Figure 19-51. A. Cohstethus

whymperí from Provincia Pichincha,
Ecuador. B. Dendrobates leucomelas
from Estado Bolívar, Venezuela.
Photos by W. E. Duellman.
EVOLUTION
542 ticulation with the coccyx, which lacks transverse processes.
The pectoral girdle is firmisternal (arciferal in a few spe-
cies of Rana); the omosternum usually is ossified, and
the sternum is ossified in most taxa (usually cartilaginous
in petropedetines). Postzonal stemal elemente are present
(except Hemisus), cartilaginous in arthroleptines and
astylosternines, and bony in others; the scapula is not
overlain anteriorly by the clavicle. Palatines are present;
a parahyoid is absent, and the cricoid ring is complete.
The maxillae and premaxillae are dentate in most groups
(edentate in hemisines, mantellines, and some arthrolep-
tines). The astragalus and calcaneum are fused only
proximally and distally; there are two tarsalia (three in
astylosternines and some petropedetines), and the pha-
langeal formula is normal (except in mantellines, in which
it is increased by the addition of short, cartilaginous in-
tercalary elements between the penultimate and terminal
phalanges). The m. sartorius is discrete from the m. semi-
tendinosus, and the tendón of the latter passes dorsal to
the m. gracilis; the m. glutaeus magnus may or may not
have an accessory tendón, and the m. adductor magnus
has an accessory head. The pupil is horizontal in most
taxa (vertically elliptical in astylosternines and hemisines).
Amplexus is axillary (modified cephalic or absent in man-
tellines). Direct development occurs in arthroleptines and
in some petropedetines and ranines; in all others, aquatic
Type IV larvae have beaks, denudes, and a sinistral spi-
racle. The trigeminal and facial ganglia are fused. The
diploid chromosome complement varíes from 14 to 54;
Figure 19-52. Distribution of living members of the family in addition, some species are polyploids.
Dendrobatidae. Ranids are extremely variable in size and habitus. Many
species are small (<50 mm snout-vent length) but Con-
raua goliath, the largest known frog, attains a length of
300 mm. Many ranids are riparian and have long legs
1868; Hyloxalus Jiménez de la Espada, 1871 and webbed feet (Occidozyga, Ptychadena, and some
Phyllodromus Jiménez de la Espada, 1875); Rana), and some have robust bodies, extensive webbing,
63 species. Costa Rica to southeastern Brazil and live in and along mountain streams (Amolops, Pe-
and Bolivia. tropedetes, Staurois, and some Rana). Others (Pyxiceph-
3. Dendrobates Wagler, 1830 (Hylaplesia Schle- a/us and Tomopterna) are toadlike, and Hemisus is fos-
gel, in Boie, 1827; Dendromedusa Gistel, sorial, whereas some P/atymantis are arboreal (Figs. 19-
1848); 48 species. Nicaragua to southeastern 53, 19-54).
Brazil and Bolivia. Silverstone (1975, 1976); Distribution.—The family is cosmopolitan except for
Myers et al. (1978). southern South America, the West Indies, the Australian
4. Phyllobates Bibron, in de la Sagra, 1841; 5 región, and most oceanic islands (Fig. 19-55). The range
species. Costa Rica to Pacific lowlands of of the Raninae is the same as the family. Four subfamilies
northwestern South America. Silverstone (Arthroleptinae, Astylosterninae, Hemisinae, and Pedro-
(1976); Myers et al. (1978). pedetinae) are restricted to sub-Saharan África, and the
Mantellinae (as used here) is endemic to Madagascar.
Fossil history.—Numerous Recent and extinct species
RANIDAE Gray, 1825 of Rana are known from late Tertiary and Quaternary
Deflnition.—There are eight holochordal, procoelous deposits in Europe and North America, and fossils re-
presacral vertebrae usually with nonimbricate neural arches ferred to Ptychadena have been reported from the Mio-
(imbrícate in astylosternines); in most taxa Presacral VIII cene of Morocco.
is biconcave and the sacrum biconvex. Presacrals I and Life history.—Most ranids deposit small, pigmented
II are not fused in most taxa (fused in Hemisus), and the eggs in quiet water and have generalized pond-type tad-
atlantal cotyles of Presacral I are widely separated. The poles, but some (e.g., Amolops) have stream-adapted
sacrum has cylindrical diapophyses and a bicondylar ar- tadpoles. Direct development of terrestrial eggs occurs in
 Classification
543

Figure 19-53. A. Arthroleptis

stenodactylus from Chisambo.
Malawi (photo by J. Visser).
B. Astylosternus bofes/ from
Cameroon (photo by J.-L. Perret).
C. Hcmisus guttatum from Natal,
South África (photo by J. Visser).
D. Mantidactylus curtas from
Ankaratra Mountains, Madagascar
(photo by R. M. Blommers-
Schlósser).

Figure 19-54. A. Cacosternum

boettgeri from Natal, South África
(photo by W. E. Duellman).
B. P/aíymanfis papuensis from Lae,
Papua New Guinea (photo by R. G.
Zweifel). C. Rana sylvatica from
Alabama, U.S.A. (photo by J. T.
Collins). D. Pfychadena anchietae
from Lake Bogoria, Kenya (photo by
J. V. Vindum).
EVOLUTION
544

Figure 19-55. Distribution of living

members of the family Ranidae.

various arthroleptínes and petropedetines, and in some ASTYLOSTERNINAE Noble, 1927

Asiatic ranines (Ceratobatrachus, Discodeles, Palmato- 4. Asfylosternus Werner, 1898 (Düobates Bou-
rappia, and Platymantis). lenger, 1900; Gampsosteonyx Boulenger,
Remarks.—Dubois (1981) considered the arthrolep- 1900); 11 species. Western África from Sierra
tines and astylosternines to represent a distínct family, León to Central African Republic and Zaire.
the Arthrolepüdae. Laurent (1979) recognized the hemi- Amiet (1977).
sines as a sepárate family and included the rhacophorines 5. Leptodactylon Andersson, 1903 (Bulua Bou-
and mantellines in the Ranidae, but placed the arthro- lenger, 1904); 11 species. Western África
leptínes and astylosternines in the Hyperoliidae. These from eastern Nigeria to southwestern Cam-
and other permutations discussed by Dubois (1981) re- eroon. Amiet (1980).
veal that the systematics of the ranoid frogs (Ranidae, 6. Nyctibates Boulenger, 1904; 1 species.
Rhacophoridae, Hyperoliidae) is in a state of chaos. The Southwestern Cameroon. Amiet (1973).
only attempt at a phylogeny is B. Clarke's (1981) work 7. Scotobleps Boulenger, 1900; 1 species. East-
on the African ranines. Some workers (e.g., Dubois, 1981) ern Nigeria to Zaire. Amiet (1973).
have recognized the nominal genus Pseudophilautus 8. Tríchobatrachus Boulenger, 1900; 1 species.
Laurent (Sri Lanka and Malabar coast of India) as a man- Eastern Nigeria to Zaire.
telline; evidence that this frog is distínct from Philautus HEMISINAE Cope, 1867
(Rhacophoridae) is not compelling, and herein Pseudo- 9. Hemisus Günther, 1859 (Kakophrynus
philautus is considered to be a synonym of Philautus. Steindachner, 1863); 8 species. Tropical and
Contení.—Different authors recognize various num- subtropical sub-Saharan África. Laurent
bers of subfamilies (see B. Clarke, 1981, and Dubois, (1972).
1981). Herein six subfamilies are recognized containing MANTELLINAE Laurent, 1946
47 living genera with 667 species; an additional 50 spe- 10. Laurentomantis Dubois, 1980 (Microphryne
cies are known only as fossils. One generic ñame, Den- Methuen and Hewitt, 1913; Trachymantis
drobatorana Ahí, 1927, with one species, cannot be placed Hewitt and Methuen, 1920); 3 species.
with certainty (Dubois, 1981). Madagascar. Guibé (1978).
11. Mantella Boulenger, 1882; 4 species. Mada-
ARTHROLEPTINAE Mivart, 1869 gascar. Busse (1981).
1. Arthroteptis Smith, 1849 (Abroscaphus Lau- 12. Mantidactylus Boulenger, 1895 (Gephyro-
rent, 1940; Coracodichus Laurent, 1940); mantis Methuen, 1920; Hylobatrachus Lau-
11 species. Sub-Saharan África. rent, 1943); 53 species. Madagascar. Blom-
2. Cardioglossa Boulenger, 1900; 16 species. mers-Schlósser (1979a).
Western and central sub-Saharan África. PETROPEDETINAE Noble, 1931
3. Schoutedenella Witte, 1921 (Arthroleptulus 13. Anhydrophryne Hewitt, 1919; 1 species.
Laurent, 1940); 20 species. Sub-Saharan Amatóla Mountains, South África. Poynton
África. (1964).
 Classification
14. Arthroleptella Hewitt, 1926; 2 species. Moun- 32. Hildebrandtia Nieden, 1907; 3 species. Trop- 545
tains of South África. Poynton (1964). ical and subtropical sub-Saharan África. B.
15. Arthroleptides Nieden, 1910; 2 species. Clarke (1981).
Mountains of Kenya and Tanzania. 33. Lanzarana Clarke, 1983; 1 species. Northern
16. Cacosíertim Boulenger, 1887; 5 species. Somalia. B. Clarke (1983a).
Eastern and southern África. 34. Micrixalus Boulenger, 1888; 13 species. China,
17. Dimorphognathus Boulenger, 1906 (Hetero- India, Sri Lanka, Borneo, and Philippines.
glossa Hallowell, 1858); 1 species. Western Pillai (1978).
África (Cameroon, Gabon, Zaire). Perret 35. Nannobatrachus Boulenger, 1882; 3 species.
(1966). Southern India.
18. Microbatrachella Hewitt, 1926 (Microbatra- 36. Nannophrys Günther, 1869 (Tmchycephalus
chus Hewitt, 1926); 1 species. Cape Fíats, Ferguson, 1875; Fergusonia Hoffmann,
South África. Poynton (1964). 1878); 3 species. Sri Lanka. B. Clarke
19. Natalobatrachus Hewitt and Methuen, 1913; (1983b).
1 species. Natal and Transkei, South África. 37. Nanorana Günther, 1896 (Montorana Vogt,
Poynton (1976). 1924); 1 species. Sichuan, China. Dubois
20. Nothophryne Poynton, 1963; 1 species. (1981)
Mountains of Malawi and Mozambique. 38. Nyctibatrachus Boulenger, 1882; 4 species.
Poynton (1963). India.
21. Petropedetes Reichenow, 1874 (Tympano- 39. Occidozyga Kuhl and van Hasselt, 1822
ceros Barboza du Bocage, 1895); 8 species. (Houlema Gray, 1831; Oxyglossus Tschudi,
Sierra León to Cameroon; Fernando Po is- 1838; Phrynog/ossus Peters, 1867; Aficro-
land. Amiet (1973). discopus Peters, 1877; Oreobatrachus Bou-
22. Phrynobatrachus Günther, 1862 (Stenorhyn- lenger, 1896; Osteosternum Wu, 1929); 9
chus Smith, 1849; Hemimantis Peters, 1863; species. Southern China to India; Greater
Leptoparius Peters, 1863; Hylarthroleptis Ahí, and Lesser Sunda Islands. Dubois (1981).
1923; Pararthroleptis Ahí, 1923; Micrarthro- 40. Pa/matorappia Ahí, 1927 (Hypsirana King-
leptis Deckert, 1938; Pseudoarthroleptis horn, 1938); 1 species. Solomon Islands. W.
Deckert, 1938); 63 species. Sub-Saharan Brown (1952).
África. 41. P/aíymantis Günther, 1859 (Halophila Gi-
23. Phrynodon Parker, 1935; 1 species. Camer- rará, 1853); 38 species. New Guinea, Phil-
oon and Fernando Po island. Amiet (1981). ippines, Bismarck, Admiralty, Palau, Fiji, and
RANINAE Gray, 1825 Solomon Islands.
24. A/tirana Stejneger, 1927; 1 species. Tibet and 42. Ptychadena Boulenger, 1917 (Límnophi/us
Nepal. Dubois (1974). Fitzinger, 1843; Abrana Parker, 1931; Par-
25. Amo/ops Cope, 1865; 23 species. North- kerana Dubois, 1984); 38 species. Sub-Sa-
eastern India, Nepal, and southern China to haran África, Madagascar, Seychelles and
the Greater Sunda Islands. Inger (1966). Mascarene islands. Miocene of Morocco.
26. Aubria Boulenger, 1917; 1 species. Gabon, 43. Pyxicepha/us Tschudi, 1838 (Ma/tzania
western África. B. Clarke (1981). Boettger, 1881; Phrynopsis Pfeffer, 1883);
27. Batrachylodes Boulenger, 1887; 8 species. 2 species. Sub-Saharan África.
Solomon Islands. W. Brown and F. Parker 44. Rana Linnaeus, 1768 (Ranada Rafinesque,
(1970). 1814; Hylarana Tschudi, 1838; Limnodytes
28. Ceratobatrachus Boulenger, 1884; 1 species. Duméril and Bibron, 1841; Lithobates Fit-
Solomon Islands. W. Brown (1952). zinger, 1843; Pelophylax Fitzinger, 1843;
29. Conraua Nieden, 1908 (Pseudoxenopus Limnonectes Fitzinger, 1843; Hydrophy/ax
Barbour and Loveridge, 1927; Gigantorana Fitzinger, 1843; EupWyctis Fitzinger, 1843;
Noble, 1931; Paleorana Scortecci, 1931; Phrynoderma Fitzinger, 1843; Zoodioctes
Hydrobatrachus Stadie, 1962); 6 species. Gistel, 1848; tAmphirana Aymard, 1855;
Tropical sub-Saharan África. Lamotte and Ránula Peters, 1860; Dicrog/ossus Cope,
Perret (1968). 1860; Hydrostentor Fitzinger, 1861; Hoplo-
30. Discode/es Boulenger, 1918; 5 species. Ad- batrachus Peters, 1863; Pohlia Steindach-
miralty, Bismarck, and Solomon islands. W. ner, 1867; Trypheropsis Cope, 1868;
Brown (1952). Pachybatrachus Mivart, 1869; C/inotarsus
31. E/achyg/ossa Andersson, 1916; 1 species. Mivart, 1869; Crotaphiíis Schulze, 1891;
Mountains of northern Thailand. E. Taylor Ba/iopygus Schulze, 1891; Levirana Cope,
(1962). 1894; Bobina Thompson, in van Denburgh,
 EVOLUTION
546 1912; tFejeruarya Bolkay, 1915; nanósoma mantis, and Tornierella); Presacral VIII is biconcave and
Ahí, 1924; Chaparana Bourret, 1939; tAn- the sacrum biconvex in all genera except Acanthixalus
chy/orana Taylor, 1942; Pao Dubois, 1975); and Callixalus. Presacrals I and II are not fused, and the
258 species. Cosmopolitan except for atlantal cotyles of Presacral I are widely separated. The
southern South America and Australia. In sacrum has cylindrical diapophyses and a bicondylar ar-
addition to many Recent species being known ticulaüon with the coccyx, which lacks transverse processes.
from the Pliocene and Pleistocene, about 50 The pectoral girdle is firmisternal; a cartilaginous or bony
extínct species are recognized from the Oli- omosternum and sternum are present, and the scapula
gocene through the Pleistocene of Europe, is not overlain anteriorly by the clavicle. Palatines are
upper Miocene through the Pleistocene of present; a parahyoid is absent, and the cricoid ring is
North America, and the Pleistocene of El complete. The maxillae and premaxillae are dentate. The
Salvador. astragalus and calcaneum are fused only proximally and
45. Staurois Cope, 1865 (Simomantis Boulen- distally; there are three tarsalia, and the phalangeal for-
ger, 1918); 3 species. Borneo and the Phil- mula is increased by the addition of short, cartilaginous
ippines. Inger (1966). intercalan; elements between the penultimate and ter-
46. Sírongy/opus Tschudi, 1838; 5 species. South minal phalanges. The m. sartorius is discrete from the m.
África northward in uplands to Tanzania. semitendinosus, and the tendón of the latter passes dor-
Greig et al. (1979). sal to the m. gracilis; the m. glutaeus magnus lacks an
47. Tomopterna Duméril and Bibron, 1841 accessory tendón, and the m. adductor magnus has an
(Sphaerotheca Günther, 1859); 12 species. accessory head. The pupil is vertically elliptical in most
Sub-Saharan África, Madagascar, and India. genera (horizontal or round in Acanthixalus, Chrysoba-
Dubois (1981). trachus, and Hypero/ius). Amplexus is axillary (inguinal
in Chrysobatrachus). All have aquatic Type IV tadpoles
HYPEROLIIDAE Laurent, 1943 with beaks and denudes; the spiracle is sinistral, and the
De/inítion.—There are eight holochordal, procoelous trigeminal and facial ganglia are fused. The diploid chro-
presacral vertebrae with nonimbricate neural arches in mosome complement is 22, 24, or 30.
most taxa (imbrícate in Cryptot/iy/ox, Kassina, Phlycti- Hyperoliids are mostly small to moderate-sized (15-82

Figure 19-56. A. Afríxalus

quadrivittatus from Lubao, Kenya
(photo by R. C. Drewes). B. Kassina
macúlate from Ukunda, Kenya
(photo by J. V. Vindum).
C. Leptopelis nordequatoriatis from
Plateau Bamileka, Cameroon (photo
by J.-L. Perret). D. Tochycnemis
seychellensis from Praslin,
Seychelles Islands (photo by J. V.
Vindum).
 Classification
mm snout-vent length) tree frogs with toe pads, but some 547
(Chrysobatrachus, Tornierella, and some Kassina) are
terrestrial (Fig. 19-56). With the exception of Acanthix-
alus, the skin is smooth. Except for Leptopelis, guiar glands
are present.
Distribution.—Most of the genera occur in sub-Sa-
haran África; Heterixalus is endemic to Madagascar, and
Tachycnemis is restricted to the Seychelles islands (Fig.
19-57).
Fossil history.—None.
Life history.—Many hyperoliids have small, pig-
mented, aquatic eggs, but A/n'xa/us and some Hyperolius
deposit unpigmented (or palé green) eggs on vegetation
above water (encased in folded leaf in Afrixalus), Acan-
thixalus lays unpigmented eggs in water in tree holes,
and Opisthothy/ax has an arboreal foam nest. Leptopelis
lays unpigmented eggs on the ground, and the tadpoles
move to ponds. Tachycnemis deposits eggs on the ground
or on stems of plants that are flooded before the tadpoles
hatch.
Remarks.—S. Liem (1970) considered hyperoliids and Figure 19-57. Distribution of living members of the family
rhacophorids to be derived independently from sepárate Hyperoliidae.
groups of ranids. Intrafamilial relationships were dis-
cussed by Drewes (1984), who provided diagnoses of
the genera. Dubois (1981) recognized three subfamilies.
Contení.—The 14 genera contain 206 species: 1924; Elaphromantis Laurent, 1941; Het-
eropelis Laurent, 1941; Taphriomantis Lau-
rent, 1941; Habrahyla Goin, 1961); 41 spe-
1. Acanfhixa/us Laurent, 1944; 1 species. cies. Sub-Saharan África. Drewes (1984).
Southern Nigeria and Cameroon to north- 11. Opisthothylax Perret, 1966; 1 species. South-
eastern Zaire. Drewes (1984). ern Nigeria to Gabon. Drewes (1984).
2. Afrixalus Laurent, 1944; 23 species. Sub-Sa- 12. Phlyctimantis Laurent and Combaz, 1950; 3
haran África. Laurent (1982); Drewes (1984). species. Southern Tanzania; western África.
3. Caí/íxa/us Laurent, 1950; 1 species. High- Drewes (1984).
lands of eastern Zaire and western Rwanda. 13. Tachycnemis Fitzinger, 1843 (Mega/ixa/us
Drewes (1984). Günther, 1869); 1 species. Seychelles is-
4. Chrysobatrachus Laurent, 1951; 1 species. lands. Drewes (1984).
Itombwe Highlands in eastern Zaire. Drewes 14. Tornierella Ahí, 1924 (fíothschi/dia Moc-
(1984). quard, 1905; Mocquardia Ahí, 1931); 2 spe-
5. Cryptothylax Laurent and Combaz, 1950; 2 cies. Central Ethiopia. Drewes (1984).
species. Cameroon to Zaire. Drewes (1984).
6. Heterixalus Laurent, 1944; 8 species. Mad- RHACOPHORIDAE Hoffman, 1932
agascar. Drewes (1984). Definition.—There are eight holochordal, procoelous
7. Hyperolius Rapp, 1842 (Eucnemis Tschudi, presacral vertebrae with nonimbricate neural arches; in
1838; Epipole Gistel, 1848; Crumenifera some taxa, Presacral VIII is biconcave and the sacrum
Cope, 1863; Rappia Günther, 1865; Nesi- biconvex. Presacrals I and II are not fused, and the at-
onixalus Perret, 1976); 109 species. Sub- lantal cotyles of Presacral I are widely separated. The
Saharan África. Laurent (1983); Drewes sacrum has cylindrical diapophyses and a bicondylar ar-
(1984). ticulation with the coccyx, which lacks transverso processes.
8. Kassina Girard, 1853 (Eremiophilus Fitzinger, The pectoral girdle is firmistemal; the omosternum, ster-
1843; Hylambates Duméril, 1853; Paracas- num, and postzonal elements are ossified, and the scap-
sina Peracca, 1907; Cossinopsis Monard, ula is not overlain by the clavicle. Palatines are present;
1937; Semnodactylus Hoffmann, 1939); 12 a parahyoid is absent, and the cricoid cartilage is com-
species. Sub-Saharan África. Drewes (1984). plete. The maxillae and premaxillae are dentate. The as-
9. Kassinula Laurent, 1940; 1 species. Zaire and tragalus and calcaneum are fused only proximally and
Zambia. Drewes (1984). distally; there are two tarsalia, and the phalangeal for-
10. Leptopelis Günther, 1859 (Pseudocassina Ahí, mula is increased by the addition of short, cartilaginous
 EVOLUTION
548 (ossified in some taxa) intercalan; elements between the of Nyctixalus, Philautus, and Theloderma lay eggs in tree
penultímate and terminal phalanges. The m. sartorius is holes and have an abbreviated, nonfeeding larval stage.
discrete from the m. semitendinosus, and the tendón of Remarks.—The relationships of rhacophorid genera
the latter passes dorsal to the m. gracilis; the m. glutaeus were discussed by S. Liem (1970). Blommers-Schlósser
magnus lacks an accessory tendón, and the m. adductor (1979a) moved the Mantellinae from the Rhacophoridae
magnus has an accessory head. The pupil is horizontal. to the Ranidae. Dubois (1981) recognized two subfami-
Aquaüc Type IV tadpoles have beaks and denticles (ab- lies.
sent in nonfeeding tadpoles of Nyctixalus, Philautus, and Contení.—Ten genera contain 186 species:
Theloderma); the spiracle is sinistral, and the trigeminal
and facial ganglia are fused. The diploid chromosome 1. Ag/yptodacty/us Boulenger, 1919; 1 species.
complement is 26. Madagascar. Blommers-Schlósser (1979a).
Most rhacophorids are arboreal frogs with enlarged toe 2. Boophis Tschudi, 1838 (Elophila Duméril and
pads, and some Rhacophorus have extensive webbing Bibron, 1841; Buccinator Gistel, 1848); 28
on the hands and feet, which gives them increased sur- species. Madagascar. Blommers-Schlósser
face área for parachuting. Some rhacophorids (Ag/yp- (1979b).
todactylus) are terrestrial (Fig. 19-58). Size varíes from 3. Buergeria Tschudi, 1838 (Dendricus Gistel,
15 to 120 mm snout-vent length. 1848); 4 species. Taiwan and Ryukyu Is-
Distribution.—Rhacophorids are widely distributed in lands to Honshu, Japan. S. Liem (1970).
the Oíd World tropics (Fig. 19-59). Seven genera occur 4. Chiríxalus Boulenger, 1893; 7 species.
in the Asían tropics and subtropics from India and Sri Southeastern Asia. S. Liem (1970).
Lanka to Japan, the Philippine Islands, and the Greater 5. Chiromantis Peters, 1863; 3 species. Tropical
Sunda Islands. Two genera are endemic to Madagascar, África.
and one is restricted to tropical África. 6. Nyctixalus Boulenger, 1882 (Hazelia Taylor,
Fossil history.—None. 1920; Eduwrdtay/oria Marx, 1975); 3 spe-
Life history.—The Madagascaran genera Aglyptodac- cies. India, Malaya, Philippines, and Greater
ty/us and Boophis have small, aquatic eggs and tadpoles. Sunda Islands. S. Liem (1970).
Buergeria, Chiromantis, Chiríxalus, Polypedates, and 7. Philautus Gistel, 1848 (Orchestes Tschudi,
Rhacophorus have foam nests (usually on vegetatíon 1838; /xa/us Duméril and Bibron, 1841;
above water) and aquatic tadpoles. At least some species Pseudophilautus Laurent, 1943); 63 spe-

Fignre 19-58. A. Ag/yptodocíy/us

madagascariensis from Madagascar
(photo by R. M. Blommers-
Schlósser). B. Boophis difficilis from
Perinet, Madagascar (photo by R. M.
Blommers-Schlósser). C. Chiríxalus
nongkhorcnsis from Thailand (photo
by K. Nemuras). D. Chiromantis
xerampelina from Natal, South
África (photo by W. E. Duellman).
 Classification
549

Figure 19-59. Distribution of living

members of the family
Rhacophoridae.

cies. India and Sri Lanka to China, the Phil- Palatines are reduced or absent in most taxa; a parahyoid
ippines and Greater Sunda Islands. S. Liem is absent, and the cricoid ring is complete. The maxillae
(1970). and premaxillae are edentate in most taxa (dentate in
8. Polypedates Tschudi, 1838 (Trachyhyas Fit- dyscophines and some cophylines). The astragalus and
zinger, 1843); 11 species. Japan and eastern calcaneum are fused only proximally and distally; there
China throughout tropical Asia to Java, Bor- are two tarsalia, and the phalangeal formula is normal in
neo, and the Philippines. S. Liem (1970). most taxa (reduced in melanobatrachines and increased
9. Rhacophorus Kuhl and van Hasselt, 1822 by the addition of short, cartilaginous intercalary ele-
(Leptomantis Peters, 1867); 56 species. In- ments between the penultimate and terminal phalanges
dia and China to Japan and the Greater in phrynomerines). The m. sartorius is discrete from the
Sunda Islands. S. Liem (1970). the m. semitendinosus, and the tendón of the latter passes
10. Theloderma Tschudi, 1838 (Phrynoderma dorsal to the m. gracilis; the m. glutaeus magnus has an
Boulenger, 1893); 10 species. China and accessory tendón, and the m. adductor magnus lacks an
Burma to Malaya and Sumatra. S. Liem accessory head. The pupil is horizontal or round (verti-
(1970). cally elliptical in dyscophines). Amplexus is axillary (males
adherent to posterior part of female in some robust spe-
MICROHYLIDAE Günther, 1859 cies). Many genera have direct development; of those
Definition.—There are eight holochordal, procoelous having aquatic larvae, they are Type II tadpoles without
presacral vertebrae with imbrícate or nonimbricate neural beaks and denticles (except scaphiophrynines and Oto-
arches; all vertebrae are procoelous ¡n cophylines and phryne); the spiracle is single and median (an elongate,
genyophrynines, but Presacral VIII is biconcave and the sinistral siphon in Otophryne), and the trigeminal and
sacrum biconvex in other subfamilies. Presacrals I and II facial ganglia are fused. The diploid chromosome com-
are not fused, and the atlantal cotyles of Presacrai I are plement is 22-28.
widely separated. Ribs are absent. The sacrum has broadly Microhylids usually are small, but some attain snout-
dilated diapophyses and a bicondylar articulation with the vent lengths of about 100 mm. The body shape vanes
coccyx (fused in some brevicipines), which lacks trans- from squat and small-headed to globular, toadlike ani-
verse processes. The pectoral girdle is firmisternal; the máis and to arboreal frogs with expanded tips of the digits
omosternum is absent in most taxa (present in brevici- (Figs. 19-60,19-61). The presence of two or three palatal
pines, cophylines, and some dyscophines and melano- folds is unique to this family, as is the fact that the nares
batrachines). A cartilaginous sternum is present, and remain closed in the tadpoles until shortly before meta-
clavicles (if present) do not overlay the scapulae ante- morphosis.
riorly (clavicles reduced, or absent in all but brevicipines). Distribution.—The family is nearly cosmopolitan in
EVOLUTION
550

Figure 19-60. A. Pseudohemisus

granulosum from Ampijoroa,
Madagascar (photo by R. M.
Blommers-Schlósser). B. Dyscophus
antongilii from Antongil Bay,
Madagascar (photo by R. M.
Blommers-Schlósser). C. Platypelis
granáis from Perinet, Madagascar
(photo by R. M. Blommers-
Schlósser). D. Phrynomantis robusta
from Sempi, Papua New Guinea
(photo by R. G. Zweifel).

Figure 19-61. A. Cophixalus

riparias from Orumba, Papua New
Guinea (photo by R. G. Zweifel).
B. Breviceps rostí from Cape
Province, South África (photo by
J. Visser). C. Phiynomerus
bífasciatus from Tasheni, Swaziland
(photo by J. Visser). D.
Elachistocleis ovale from Estado
Táchira, Venezuela (photo by W. E.
Duellman).
 Classification
551

Figure 19-62. Distribution of the

living members of the family
Microhylidae.

températe and tropical regions, except for the Palaearctic graphic grounds. Zweifel (1971) provided morphological
Región, most of Australia, the West Indies, and most evidence to support the recognition of the Asterophryi-
oceanic islands (Fig. 19-62). The Asterophryinae is re- nae and Genyophryninae. The Melanobatrachinae may
stricted to the Australo-Papuan región, where the Geny- be polyphyletic (J. Savage, 1973). Much of the basic
ophryninae is most diverse, but also occurs in Célebes, information on microhylids is derived from H. Parker's
Lesser Sunda Islands, and southern Philippine Islands. (1934) monograph. More recent reviews are of South
The Cophylinae and Scaphiophryninae are endemic to American microhylines (Carvalho, 1954), asterophryines
Madagascar, and the Dyscophinae occurs in Madagascar (Zweifel, 1972a), and Madagascaran genera (Guibé,
and southeastern Asia. The Microhylinae is widespread 1978).
in the New World and southeastern Asia and adjacent Contení.—Nine subfamilies contain 61 genera with 279
islands; the Brevicipinae and Phrynomerinae are re- species:
stricted to sub-Saharan África, a región also inhabited by
the Melanobatrachinae, which also occurs in India. SCAPHIOPHRYNINAE Laurent, 1946
Fossil history.—The only fossils referable to this fam- 1. Pseudohemisus Mocquard, 1895; 6 species.
ily are those of Gastrophryne from the Miocene of Flor- Madagascar. Guibé (1978).
ida, U.S.A. (Holman, 1967). 2. Scaphiophryne Boulenger, 1882; 1 species.
Life history.—Most microhyline genera and phrynom- Madagascar. Guibé (1978).
erines have small, pigmented, aquatíc eggs and free- DYSCOPHINAE Boulenger, 1882
swimming tadpoles with small terminal mouths lacking 3. Callueh Stoliczka, 1872 (Colpoglossus Bou-
beaks and denudes. A dorsal funnel-shaped mouth is lenger, 1904; Dyscophina van Kampen,
present in some Asiatic species Microhyla and Kalophry- 1905; Calliglutus Barbour and Noble, 1916);
nus. Direct development of terrestrial eggs occurs in all 5 species. Southeastern Asia and Malay Ar-
asterophryines and genyophrynines and in some micro- chipelago to Borneo. Inger (1966).
hylines (Myersietla and presumably also in Synaptur- 4. Dyscophus Grandidier, 1872; 3 species.
anus). In Breviceps and Hoplophryne terrestrial eggs hatch Madagascar. Guibé (1978).
into nonfeeding tadpoles that complete their develop- COPHYLINAE Cope, 1889
ment within the nest. Knowledge of the life histories of 5. Anodonthyla Müller, 1892; 3 species. Mad-
many genera is lacking. agascar. Guibé (1978).
Remarles.—Both larval and adult morphology distin- 6. Cophyla Boettger, 1880; 1 species. Northern
guish microhylids from other families of anurans. How- Madagascar. Guibé (1978).
ever, the relationships among the nine subfamilies are 7. Madecassophryne Guibé, 1974; 1 species.
obscure. J. Savage (1973) combined the Asterophryinae Madagascar. Guibé (1978).
and Genyophryninae ( = Sphenophryninae) into one 8. Mantipus Peters, 1883 (Mantiphrys Moc-
subfamily and made other changes in the contents of quard, 1895); 7 species. Madagascar. Guibé
subfamilies; these changes were made mostly on geo- (1978).
EVOLUTION
552 9. Paracophy/a Millot and Guibe, 1951; 1 spe- BREVICIPITINAE Bonaparte, 1850
cies. Eastern Madagascar. Guibé (1978). 27. Breviceps Merrem, 1820 (Systoma Wagler,
10. Plafypelis Boulenger, 1882 (Pfaryhy/a Bou- 1830; Engystoma Fitzinger, 1843); 12 spe-
lenger, 1889); 9 species. Madagascar. Guibé cies. Southern África. Poynton (1964).
(1978). 28. Ca/íu/ina Nieden, 1910; 1 species. Mountains
11. P/ethodontohyla Boulenger, 1882 (Phryno- of Tanzania.
cara Peters, 1883); 7 species. Madagascar. 29. Probreuiceps Parker, 1931; 3 species. East-
Guibé (1978). ern África.
12. Rhombophryne Boettger, 1880; 1 species. 30. Spelaeophryne Ahí, 1924; 1 species. Eastern
Madagascar. Guibé (1978). Tanzania.
13. Stumpffia Boettger, 1881; 5 species. Mada- MELANOBATRACHINAE Noble, 1931
gascar. Guibé (1978). 31. Hoplophryne Barbour and Loveridge, 1928;
ASTEROPHRYINAE Günther, 1859 2 species. Mountains of Tanzania.
14. Asterophrys Tschudi, 1838; 1 species. New 32. Melanobatrachus Beddome, 1878; 1 species.
Guinea. Zweifel (1972a). Southwestern India.
15. Barygenys Parker, 1936; 7 species. Moun- 33. Parhoplophryne Barbour and Loveridge,
tains of western Papua New Guinea and 1928; 1 species. Usambara Mountains, Tan-
Louisiade Archipelago. Zweifel (1972a). zania.
16. Hy/ophorbus Macleay, 1878 (Metopostira PHRYNOMERINAE Noble, 1931
Mehely, 1901); 1 species. Papua New 34. Phrynomerus Noble, 1926 (Brachymerus
Guinea. Zweifel (1972a). Smith, 1847; Fichteria Scortecci, 1941); 4
17. Pherohapsis Zweifel, 1972; 1 species. Papua species. Sub-Saharan África.
New Guinea. Zweifel (1972a). MICROHYLINAE Günther, 1859
18. Phrynomantis Peters, 1867 (Mantophryne 35. Arcovomer Carvalho, 1954; 1 species.
Boulenger, 1897; Gnaíhophryne Mehely, Southeastern Brazil. Carvalho (1954).
1901; Pomaíops Barbour, 1910); 15 spe- 36. Chaperína Mocquard, 1892; 1 species. Malay
cies. New Guinea, Moluccan islands, and Península, Borneo, and the Philippines. In-
Louisiade Archipelago. Zweifel (1972a). ger (1966).
19. Xenobatrachus Peters and Doria, 1878 37. Chiosmoc/eis Mehely, 1904 (Nectodacty/us
(Choanacantha Mehely, 1898); 9 species. Miranda-Ribeiro, 1924); 12 species. Cis-
New Guinea. Zweifel (1972a). Andean South America and Panamá.
20. Xenorhina Peters, 1863 (Callulops Boulen- 38. Ctenophryne Mocquard, 1904; 1 species.
ger, 1888; Pseudengysfoma Witte, 1930); 6 Northern cis-Andean South America.
species. New Guinea and Louisiade Archi- 39. Dosypops Miranda-Ribeiro, 1924; 1 species.
pelago. Zweifel (1972a). Coast of eastern Brazil.
GENYOPHRYNINAE Boulenger, 1890 40. Dermatonotus Mehely, 1904; 1 species.
21. Choerophryne van Kampen, 1915; 1 species. Northeastern Brazil to Chacean Argentina
New Guinea. Menzies and Tyler (1977). and Bolivia. Cei (1980).
22. Cophixalus Boettger, 1892 (Phryn¡xa/us 41. Elachistocleis Parker, 1927; (Microps Wagler,
Boettger, 1895; Aphantophryne Fry, 1917); 1828; Stenocephalus Tschudi, 1838); 4
23 species. New Guinea, Moluccas islands, species. Cis-Andean South America south to
and northeastern Queensland, Australia. Argentina; Panamá.
Zweifel (1979); Cogger et al. (1983). 42. Gastrophryne Fitzinger, 1843; 5 species.
23. Copiu/a Mehely, 1901; 3 species. New Guinea. Southern United States to Costa Rica. C.
Menzies and Tyler (1977). Nelson (1972).
24. Genyophryne Boulenger, 1890; 1 species. 43. Gastrophrynoides Noble, 1926; 1 species.
Eastern Papua New Guinea. Zweifel (1971). Borneo. Inger (1966).
25. Oreophryne Boettger, 1895 (Mehe/yía Wan- 44. G/ossostoma Günther, 1900; 2 species. Low-
dolleck, 1911); 24 species. Southern Phil- lands of Costa Rica to western Ecuador;
ippine Islands, Célebes, Lesser Sunda Is- Andes of Ecuador.
lands, New Guinea, and New Britain. Inger 45. G/yphog/ossus Günther, 1868; 1 species.
(1954); Zweifel (1956). Southeastern Asia. E. Taylor (1962).
26. Sphenophryne Peters and Doria, 1878 (Lio- 46. Hamptophryne Carvalho, 1954; 1 species.
phryne Boulenger, 1897; Microbatrachus Amazon Basin, South America. Duellman
Roux, 1910; Austrochaperina Fry, 1912; (1978).
Oxydacíy/a van Kampen, 1913); 17 species. 47. Hyophryne Carvalho, 1954; 1 species.
New Guinea, New Britain, and extreme Northeastern Brazil.
northern Australia. Cogger et al. (1983). 48. Hypopachus Keferstein, 1867; 2 species.
 Classification
Southern Texas, U.S.A., and Sonora, México, ported species from Madagascar. 553
to Costa Rica. C. Nelson (1973a). 53. Myersie/ía Carvalho, 1954; 1 species. South-
49. Ka/ophrynus Tschudi, 1838 (Calophryne Fit- eastern Brazil.
zinger, 1843; Berdmorea Stoliczka, 1872); 54. Otophryne Boulenger, 1900; 1 species.
9 species. Southern China to Borneo and Guianan región of northem South America.
the Philippines. Inger (1966). 55. Phryne/ía Boulenger, 1887; 1 species. Malay
50. Ka/ou/a Gray, 1831 (Hy/adacty/us Tschudi, Península and Sumatra.
1838; P/ecíropus Duméril and Bibron, 1841; 56. Ramane//a Rao and Ramanna, 1925; 8 spe-
Ca/ohy/a Peters, 1863; Ho/onectes Peters, cies. Southeastern India and Sri Lanka.
1863; Ca//u/a Günther, 1864; Hy/ophryne 57. Relictiuomer Carvalho, 1954; 1 species. Pan-
Fitzinger, in Steindachner, 1864; Caco- amá and northern Colombia.
poides Barbour, 1908); 9 species. Korea and 58. Stereocyc/ops Cope, 1870 (Emydops Mi-
northern China to Lesser Sunda Islands, randa-Ribeiro, 1920; Ribeirina Parker, 1934);
Philippines, and Sri Lanka. 1 species. Coast of eastern Brazil. Cochran
51. Metaphrynella Parker, 1934; 2 species. (1955).
Southern Malay Península and Borneo. In- 59. Synapturanus Carvalho, 1954; 3 species.
ger (1966). Colombia eastward to eastern Brazil.
52. Microhy/a Tschudi, 1838 (Siphneus Fitzinger, 60. Syncope Walker, 1973; 2 species. Amazon
1843; Dendromanes Gistel, 1848; Dip/o- Basin in Ecuador and Perú.
pelma Günther, 1859; Scaptophryne Fitzin- 61. Uperodon Duméril and Bibron, 1841 (Hy-
ger, 1861; Copea Steindachner, 1864; Ran- perodon Agassiz, 1846; Cacopus Günther,
ina David, 1872); 21 species. Ryukyu Islands 1864; Pachybatrachus Keferstein, 1868); 2
and China south through India to Sri Lanka, species. India and Sri Lanka.
and southeastern Asia to Bali; one pur-
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M

=
Wunderer, H.
Wunderer, H.: embiyonic development Xenopus laevis—cont. Xenorhina, 552
and metabolism, 117, 128 appendicular muscles, 349 Xiphoctonus, 506
Wurst, G. Z.: caecüian teeth, 309 color pattern, genetic mutations, 456 Xiphonura, 506
Wyman, R. L.: salamander vocalization, cranium, sequence of ossification, 183
87 effect of introduction, 8
eggs: clutch structure, 112
developmental time and tempera-
ture, 122 Yager, D. D.: anuran vocalization, 91
effects of ultraviolet irradiation, 114 Yamaguti, S.: parasites, 242
hatching, 136 Yanev, K. P.: biochemical systematics and
Xavier, F.: anuran development, 15, 129 embryos: development, 109 temporal evolution, 457
embryonic gills and metabolism, 117, nitrogenous wastes, 120 Plethodontidae, 507
125-126 rate of development, 136 Yang, S. Y.: population genetics, 457
Xenobatrachus, 552 genome size, 454-455 Yarnell, R. M.: anuran courtship and
Xenodon: predation, 245, 260 inner ear, 388 mating, 81
Xenodon severus: predation, 245 integument: biochemistry, 370 Yolk: constituents, 14
Xenophrys, 524 vascularization, ZOO reserves, 23, 168
Xenopus, 522 water flux, 200 Yorke, C. D.: parasites, 243
biogeography, 489-490 larvae: phototaxis, 163 survivorship, 283
cardiac circulation, 400 respiration, 165 Young, A. M.: predators, 244
chromosome complement, 448, 473, schooling, 169-171
521 structure, 159
cranial nerves, 393 longevity, 265
cranial osteology, 317 mesoderm formation, 443 Z
dentition, 319 metamorphosis: albumins, 179 Zachaenus, 531
genome size, 454 experimental hormonal control, 173 reproduction, 529
gilí development, 125 eye, 181 Zachaenus parvus: parental care, 41
goblet cells, 184 gut, 186 Zaisanurus, 498
heart, 399 hemoglobins,180 Zaphrissa, 524
histones in spermatozoa, 111 hypothalamic-pituitary control, 177 Zhao, E.: Chínese amphibians, 4
integumentary keratinization, 372 interrenal activity, 175 Cryptobranchidae, 498
intrageneric relationships, 457 nervous system, 188 Hynobiidae, 497-498
larvae: feeding, 162, 167 neuromasts, 184 Salamandridae, 504-505
respiration, 164-165 thyroxin levéis, 175 Zimmerman, B.: anuran reproduction, 23
structure, 159 TSH, 176 Zimmermann, E.: anuran reproduction,
locomotion, 356 nitrogen excretion, 206-207 45, 70-71, 85, 162
mesoderm formation, 443 normal stages of development, 128 Zimmermann, H.: anuran reproduction,
muscles: appendicular, 360 oocyte growth, 16 45, 70-71, 85, 162
axial, 333 osmoregulation, 207-209 Zoodioctes, 545
thigh, 471 parasitism by Chlamydocephalus, 242 Zuber-Vogeli, M.: metamorphosis, 176
nitrogen excretion, 206-207 pectoral girdle, 347 Zug, G. R.: anuran locomotion, 5
Nobelian rods, 78 predation on tadpoles and anurans, anuran reproduction, 37, 169
oviposition, 73 244 movements and home range, 265
pelvic girdle, 356 reproduction, 15, 21 parasites, 243
prey capture, 237 respiration, 218, 220 population biology, 268, 272
relationships, 522 ribosomal DNA, 455 thermal biology, 213, 216-217, 226
reproductive mode, 23 sex determination, 447, 450 Zug, P. B.: anuran reproduction, 37, 169
respiration, 220 territorial behavior, 267 movements and home range, 265
structure, 520-521 ultimobranchial bodies, absence, 177 parasites, 243
ultimobranchial bodies, absence of, vascular system, 401, 402-403 population biology, 268
413 viral infections, 241 thermal biology, 213, 216-217, 226
vascular system, 404 water economy: loss, 204 Zweifel, R. G.: anuran chromosomes, 449
vascularization: hormonal control, 200 storage, 201 anuran reproduction and vocalization,
integument, 200 Xenopus ruwenzoriensis: advertisement 24, 43, 55, 89, 94, 98, 104, 115
Xenopus borealis: laryngeal structure, 91 cali, 98 Australo-Papuan anurans, 6
Xenopus gilli, 521 polyploidy, 451 embryonic temperature tolerances,
Xenopus laevis: adhesive glands, func- Xenopus tropicalis: chromosome comple- 123-124
tion, 127 ment, 448 Microhylidae, 551-552
advertisement cali, 98 genome size, 454 Myobatrachidae, 526
androgens in tonas semicircularis, 97 Xenopus vestitus: polyploidy, 451 Zylberberg, L.: caecilian scales, 374

670
Library of Congress Cataloging-in-Publication Data

Duellman, William Edward, 1930-

Biology of amphibians / William E. Duellman, Linda Trueb.
p. cm.
Originally published: New York : McGraw-Hill, © 1986. With new pref.
Includes bibliographical references and Índex.
ISBN 0-8018-4780-X
1. Amphibians. I. Trueb. Linda. II. Title.
QL667.D84 1994
579.6—dc20 93-24401
LIFE SCIENCES A JOHNS HOPKINS PAPERBACK

"Duellman and Trueb truly review the biology of amphihians,

covering most conceivable topics from cytogenetics and development
to bio-geography and phylogeny. . . . There is no recent textbook on
ampbibian biology that is worthy of comparison."—Science

This is the widely acclaimed, pre-eminent reference and text on all

aspects of amphibian biology, including their life history, ecology,
morphology, and evolution. Copiously illustrated with original
drawings and photographs and meticulously referenced with more
t han 2,500 bibliographic entries, it has proved indispensable to
professional biologists and students alike. Now re-issued in paperback
with an updated preface by the authors, Biology ofAntphibiaiu remains
the standard work in its fíeld.

"An impressive review of current knowledge concerning all aspects

of amphibian biology. The authors have organized a tremendous
number of facts, observations, and theories around the complementary
themes of structure and evolution. . . . A major undertaking."
—Bio<fcience

"The text is clear and concise and richly illustrated. . . . This book
goes some way towards being all one could wish for and is likely to
be an important source of reference."—Na.tu.re

William E. Duellman and Linda Trueb are curators in the división

of herpetology at the Museum of Natural History, University of
Kansas, Lawrence.

The Johns Hopkins University Press ISBN 0-fl01fl-M7flO-X

Baitimore and London
90000
Cover design by Julio Burris
Cover photo: fíy/a pieturata.
Photo by William E. Duellman
9"780801"847806"