BOOK OF BIRDS

Gideon Lincecum Nature & Environment Series

Sponsored by Jerry B. Lincecum
and Peggy A. Redshaw

1stPages_A.indd 1 7/22/20 10:26 AM

1stPages_A.indd 2 7/22/20 10:26 AM
 BOOK
of
BIRDS
Introduction to Ornithology

John Faaborg

Illustrations by Claire Faaborg

TEXAS A&M UN I V ER S I TY PRE SS    COLLE GE STAT ION

1stPages_A.indd 3 7/22/20 10:27 AM

 Copyright © 2020
by John Faaborg,
illustrations by Claire Faaborg
All rights reserved
First edition

This paper meets the

requirements of ANSI/​NISO Z39.48–1992
(Permanence of Paper).
Binding materials have been
chosen for durability.

Printed in Canada by Friesens.

Library of Congress Cataloging-in-Publication Data

Names: Faaborg, John, 1949– author. | Faaborg, Claire, illustrator.

Title: Book of birds: introduction to ornithology / John Faaborg;
illustrations by Claire Faaborg.
Other titles: Gideon Lincecum nature and environment series.
Description: First edition. | College Station : Texas A&M University
Press,
[2020] | Series: Gideon Lincecum nature and environment series |
Includes bibliographical references and index. | Summary: “In this
beautifully illustrated volume, Faaborg’s approachable writing style
will engage students and birders alike while introducing them to the
study of the evolution, taxonomy, anatomy, physiology, diversity, and
behavior of birds. With its unique focus on ecology, the text emphsizes
birds’ relationships with the environment and other species while
showing the amazing diversity of avian life”—Provided by publisher.
Identifiers: LCCN 2019034266 (print) | LCCN 2019034267 (ebook) |
ISBN 9781623497767 (hardcover) | ISBN 9781623497774 (ebook)
Subjects: LCSH: Ornithology. | Birds--Ecology.
Classification: LCC QL673 .F27 2020 (print) | LCC QL673 (ebook) |
DDC
598—dc23
LC record available at https://lccn.loc.gov/2019034266
LC ebook record available at https://lccn.loc.gov/2019034267

1stPages_A.indd 4 7/22/20 10:27 AM

 With gratitude for her long commitment
to the mission of Texas A&M University Press,
her colleagues,
the Press’s Faculty Advisory Committee,
and its Advancement Board
publish this special book
in appreciation and honor of
SHANNON DAVIES,
the Press’s distinguished director,
upon her retirement.

1stPages_A.indd 5 7/22/20 10:27 AM

1stPages_A.indd 6 7/22/20 10:28 AM
 CONTENTS

Preface ix

Acknowledgments xi

Chapter 1. An Introduction to Ornithology 1

Chapter 2. General Traits of an Avian Flying Machine 19

Chapter 3. Flight 65

Chapter 4. Speciation and Radiation 83

Chapter 5. Constraints on Avian Diversity 126

Chapter 6. Systematics and Taxonomy: Classifying Birds 155

Chapter 7. Foraging Behavior 187

Chapter 8. Adaptations for Survival in Extreme Environments 216

Chapter 9. Migration 239

Chapter 10. Anatomy and Physiology of Reproduction 279

Chapter 11. General Patterns of Reproductive Behavior 310

Chapter 12. Adaptive Variation in Avian Reproduction 345

Chapter 13. Economic and Cultural Values of Birds 390

Notes 409

Bibliography 415

Suggested Reading 431

Index 437

1stPages_A.indd 7 7/22/20 10:28 AM

1stPages_A.indd 8 7/22/20 10:28 AM
 PREFACE

Obviously, this book deals with ornithol- in anatomy, morphology, and behavior
ogy, which is quite simply the study of that exists in the world of birds. To avoid
birds. But ornithology is an exceedingly writing an 800-page book, I put little
broad topic, particularly if you include emphasis on such topics as internal
all the conservation-related work done anatomy, physiology, and neurobiology,
on birds in recent decades. A recently and more on the role of competition,
produced “handbook” of bird biology is community structure, and reproductive
so long (1302 pages) that each chapter behavior in driving nature to produce
starts with page 1. The most recent best such an amazing diversity of birds
seller in ornithology is a book of nearly around the world. With this ecological
800 pages. As a university teacher, I approach, I hope that after reading this
have found those options to be too much book, you better understand how the
material to cover in a semester, particu- birds in your life work. Why does that
larly when we also have laboratory exer- blackbird have such a red shoulder?
cises, and also pretty expensive, when Why is that robin attacking your win-
we also force students to buy field guides dow? What are those bird chirps that
and binoculars for the labs. On the you hear late at night during spring and
other hand, a recent book from England fall migration?
attempted to cover “essential” ornithol- One of the most important things I
ogy in just 167 pages, which appeared to would like you to understand with this
miss too many interesting topics for me. book is why a bird looks the way it does.
Based on my having taught ornithology Birds have evolved almost unbelievable
and avian ecology courses for 40 years, I patterns of color and shape as part of
have attempted to provide a book that is their reproductive behavior. There is no
reasonably comprehensive, but not too other animal group with quite as much
big and not too expensive, and that has variation in color as birds, and by using
just the right mix of topics. color in most of the graphics in this
Which brings us to the “ecologi- book, we hope to visually give you some
cal approach” in the title. My editors sense of that variation while explaining
often asked me, “What is an ecological it in the text. With modern access to the
approach to ornithology?” My response internet and the amazing photographs
was that it is really an ecological and available there, we do not attempt to
evolutionary approach to understanding compete with photographs; rather, my
birds, but that including both topics in daughter, Claire, and I hope to give you
the title would be too confusing. My goal a visual sense of what is going on as you
is to try to show the diversity of birds in read the text and begin to understand
a way that explains why such diversity the variation that is the world of birds.
exists and how these diverse forms can
coexist, using all the wonderful variation

1stPages_A.indd 9 7/22/20 10:28 AM

1stPages_A.indd 10 7/22/20 10:29 AM
 ACKNOWLEDGMENTS

A larger version of this textbook first an old friend from bird meetings,
appeared in the late 1980s as Ornithol- Shannon Davies, who had developed
ogy: An Ecological Approach. At that time, an impressive list of bird books for the
the ornithology books that were available University of Texas Press before she
tended to be much more laboratory and moved to Texas A&M University Press.
museum oriented, which reflected the We felt that there was a market for my
state of the science of ornithology at that kind of ornithology book, one that was
time. The goal of my book was to be fairly comprehensive but not too large
both comprehensive in scope (covering or expensive. We also hoped it would be
all of ornithology) and to incorporate easy to read and could be marketed not
all of the new discoveries made about only to undergraduates but to anyone
avian ecology and evolution during the who might be interested in understand-
1970s and 1980s that were not in the ing birds.
textbooks available to me when I was in For a while, we were hung up on
school. Because my university taught the sort of design we might want. As
ornithology at a sophomore-junior level, it turned out, while we were discuss-
I also wanted a book that was fairly com- ing options, my daughter, Claire, was
prehensive but not as large as the older growing up and developing spectacular
books or the new ornithology books that artistic abilities. With formal training
appeared at the same time as mine. in art history and lots of experience
My original publisher was bought being dragged into the field with her
out by a larger publisher who was not father, Claire showed tremendous talent
as enthusiastic about this text as I had at doing bird and other science illus-
hoped, so after a single printing my tration. With some great examples, we
publisher dropped its support. I was convinced Shannon that a textbook done
able to round up enough copies to teach almost completely with hand-drawn art
ornithology on campus for a few years, would allow us to fulfill the goals of a
but it was difficult. About 15 years ago, textbook art program while also being
our book store developed the ability to colorful and attractive. Thus, we have an
make books on campus, and I immedi- unusual father-daughter textbook.
ately converted 12 of the original chap- My colleague Susan Chaplin, who
ters into a short but decent quality text. was at the University of Missouri for
It also was very cheap, which made the some time, helped with major parts of
students happy, particularly when they the first version of this book. She was
also had to buy field guides, lab manu- originally listed as a coauthor for chap-
als, and binoculars for this class. I used ters 2, 9, and 11, although she helped
various versions of this book for many with other parts of the book. She is
years, updating chapters every few years. responsible for much of the anatomy
A few years ago, I was talking with and physiology in this book, although

1stPages_A.indd 11 7/22/20 10:29 AM

 I should be blamed for any mistakes in writes, “Without John Faaborg as a
this version. father, I might never have known about
I have many people to thank for or painted the iridescence in the wing
their help on this revision. Mark Ryan of a Myna, the piercing gaze of a Hawk
was very helpful with the first version Eagle, or the spirited dance of a Grebe.
of the text, but most of the changes in It is both because of and for him that I
the uncounted number of revisions have illustrated this book.”
were comments from undergrads who We thank Shannon Davies of Texas
volunteered to do some extra editing. A&M University Press for many years of
Heather Tearney of the university support while the book developed in our
bookstore at the University of Missouri minds. Katie Duelm, Mary Ann Jacob,
helped us develop the sample books that and all the other behind-the-scenes
were modified over time. Claire did an personnel at TAMU Press, as well as
impressive amount of art; every father copyeditor Laurel Anderton, helped put
should have the chance to work with his the pieces together and move the book
daughter on a bird book. Maybe. Work- through production and publication.
ing with Claire on this project has been My wife, Janice, has dealt with my
one of my favorite lifetime memories. joys and frustrations regarding this text
Claire would like to thank her for most of our married life. Adding our
public school art teachers, whose years daughter to the mix has been, in gen-
of tutelage, encouragement, and pur- eral, a wonderful thing, although none
loined classroom art supplies contrib- of this happened fast. We do think that
uted directly to this project. She’d also the mix of text and art explains things
like to thank me, though I told her you and entertains at the same time. Hope
shouldn’t thank one’s coauthors. She you agree.

1stPages_A.indd 12 7/22/20 10:29 AM

 BOOK OF BIRDS

1stPages_A.indd 13 7/22/20 10:29 AM

1stPages_A.indd 14 7/22/20 10:29 AM
 C HA PT E R 1

An Introduction
to Ornithology

T
he term “ornithology” has double circulation is a trait shared with
its roots in the Greek ornis, mammals (which have the aortic arch on
“birds,” and logos, “the study the left side). Such a system seems to be
of.” Thus, ornithology is a necessary part of maintaining homeo-
simply the study of birds. Long, complex thermy (warm-bloodedness), another
definitions of ornithology have been trait shared by birds and mammals. Birds
offered, but these are unnecessary. Any are distinctive in their highly developed,
study that deals with birds is ornithol- powered flight and its diverse forms, but
ogy, although it might also be considered among the mammals, bats are also excel-
ecology, paleontology, behavior, or some lent fliers. Additionally, the evolution of
other branch of science. wings has led to bipedal walking in birds,
Today’s birds comprise the class a trait that has become so developed in
Aves of the subphylum Vertebrata and some forms that the powers of flight have
phylum Chordata. The other primarily been lost. While most mammals and
terrestrial vertebrates with which birds reptiles are quadrupedal, bipedalism is
currently share the world are the rep- obviously not purely an avian trait. Some
tiles (class Reptilia), mammals (class authors make a big deal about the beak, a
Mammalia), and terrestrial amphibians feature of birds shared only by the beaked
(class Amphibia) such as salamanders. mammalian Duck-billed Platypus (Orni-
While virtually everyone can recognize thorhynchus anatinus).
a bird, a close examination of these When compared to modern rep-
three groups of animals has historically tiles (excluding the crocodile, which as
shown only two distinctly avian traits. we will see is an exceptional reptile),
The most obvious of these is the covering mammals and birds are distinctive in
of feathers found on all birds. Although the relatively large amount of care that
sharing the same origin and composition parents provide their offspring. Whereas
as lizard scales, feathers are very different this care in most mammals is directed
from the scales of lizards or the hair of toward young that are born alive, the
mammals. The other distinct avian trait existence of such primitive egg-laying
is the presence of a right aortic arch that mammals as the platypus and Spiny
carries pure blood from the heart to the Echidna (Tachyglossus aculeatus) again
body. While the location of this arch is reduces the distinctiveness of the avian
distinctive, the four-chambered heart with reproductive system.

1stPages_A.indd 1 7/22/20 10:29 AM

 Among living forms, it is the reptiles mammals), but there was a period when
that share the most traits with birds. The at least two major types of dinosaurs
scales covering most reptiles are identi- dominated land animal communities.
cal in general composition to the scales Of course, in all these cases, the original
on bird legs and some bird beaks.1 The forms that separated from a common
egg of reptiles and birds is much the ancestor looked quite different from
same, and both have young that use an the forms they became over millions
“egg tooth” to crack the shell to emerge. of years of evolution. Additionally, the
The general internal arrangement of fossil record did not always record these
organs is similar, and the air sacs of forms, or it left only a record of bones
birds are placed in a manner similar to for us to use to try to re-create history.
that of the air sacs of turtles and chame- Thus, in recent years, a serious (and
leons. A number of skeletal traits are often rancorous) argument has devel-
shared by these groups, including the oped about the origins of birds, with two
bone at the skull-neck hinge (the occipi- major theories involved, one supported
tal condyle), the basic jaw structure, the mostly by the old-school, classically
lateral brain case, the structure of over- trained, mostly near-retirement types,
lapping ribs, the intertarsal ankle joint, and the other by younger faculty who
and the presence of a single bone in the like to think outside of what they see as
middle ear. Birds are particularly similar the traditional box.
to crocodiles in the structure of the pleu- To understand the origins of birds,
ral (body) cavity, the shape and structure we need to take a brief look at avian pale-
of the brain, the inner ear structure, and ontology, the study of the fossil record of
the characteristics of the blood proteins. birds. All paleontology faces problems
Parental care is also shared only with associated with the chance occurrence
the crocodiles among the present-day of fossilization, with no guarantees that
reptiles. the bones or other evidence discovered
represent a cross section of the animals
Origins of Birds: A Look at living at a particular time. Most fossils
Avian Paleontology are best preserved in such sediments as
lake beds or ocean bottoms, a character-
With so many similar characteristics, it istic that immediately biases the fossil
is not surprising that birds share a closer record toward aquatic forms and away
evolutionary history with reptiles than from land-dwelling forms, especially
with mammals. Yet, to think of birds those of the dry uplands. Generally, only
as “hot-blooded reptiles” derived from hard parts, particularly large bones, are
forms we see today is misleading and preserved, so little can be said about
simplistic. It is clear that ancestors of soft internal structures, skin color, and
birds and present-day reptiles diverged similar features. Since birds are gener-
millions of years ago, at about the same ally small and have light, often hollow,
time as mammals arose from a common bones, it is not surprising that bird
chapter 1

ancestor. From this radiation came the fossils are hard to find. On the other
groups we still see today (birds, tur- hand, it has been suggested that our
tles, snakes, lizards, crocodilians, and knowledge of bird evolution is presently

1stPages_A.indd 2 7/22/20 10:29 AM

 limited more by the scarcity of paleor- modern birds (most agree it does not),
nithologists than by the lack of fossils. but simply that it is the oldest-known
At one point in the past, only 15 authors bird in the fossil record. There have
were responsible for three-fourths of been some claims of a fossil (Protoavis)
the published descriptions of fossil that is as much as 75 million years older
species2,but this has changed somewhat than Archaeopteryx, but the consensus
recently. In particular, a great many new still favors Archaeopteryx as the oldest
fossils have come from China in recent bird. Let us examine these two general
years, in deposits that are fine enough to areas of agreement before we look at the
preserve the detail of bird skeletons and two major arguments for the evolution
even feathers. of birds.
The difficult fossilization process
for birds has resulted in relatively little The reptilian ancestry of birds
information about fossil birds. The same
undoubtedly holds true for any small, To understand the separation between
fragile reptilian forms from which birds modern reptiles and birds, we need to
might have evolved. With this paucity go back about 300 million years to the
of information, it is not surprising that end of the period known as the Carbon-
paleornithologists disagree about the iferous. At this time, the first reptiles
origins of birds and have been doing so (order Cotylosauria; fig. 1.1) had recently
for at least 150 years. Nearly 30 years been derived from amphibian forms.
ago, a reviewer of a volume titled The These early reptiles were amphibious in
Beginnings of Birds 3 suggested that “this general behavior, but they had evolved
volume has more arguments per page an egg that could be laid and would
than I have seen in a long time.”4 develop on land. The development of
To an ecologist reading the paleor- this egg meant that these early reptiles
nithological literature, it appears as if were no longer forced to be near water,
there are only two topics about which which allowed them to penetrate large
paleornithologists agree concerning landmasses. Because the terrestrial
the origins of birds. First, they agree environment was essentially unfilled at
that birds separated from the line of this time, a variety of evolutionary devel-
present-day lizards, snakes, and turtles opments occurred. The cotylosaurs are
very early in the evolutionary sequence. considered the “stem reptiles” because
Therefore, to understand the evolu- all reptilian forms arose from them, plus
An Introduction to Ornithology

tion of birds, we must go back to the the mammals and birds.

beginning of the radiation of terrestrial In part because of their rapid varia-
animals on this planet. This radiation tion and adaptation to these new terres-
also included the traditional dinosaurs, trial conditions, the stem reptiles rather
which dominated the earth for millions quickly disappeared as they evolved
of years but are now completely gone. into a diversity of better-adapted forms.
Second, they agree that Archaeopteryx is One of the earliest separations was a
the earliest-known fossil that can be clas- set of primitive reptiles that led to what
sified as a bird. This does not imply that are present-day mammals. Depending
it serves as the primitive ancestor for all on when one decides the mammal-like

1stPages_A.indd 3 7/22/20 10:29 AM

 Fig. 1.1. Radiation of
land animals from the
early reptiles (order
Cotylosauria) to
present-day groupings.
The first split involved
separation of mammals
and thecodonts, which
radiated into the highly
diverse ruling reptiles.
Note that birds may
have evolved directly
from thecodonts,
through crocodilians, or
through the sauropod
dinosaur group.

reptiles became true mammals, the ant separation of the stem reptiles led
class Mammalia may be older than the to two major divisions of land-dwelling
class Aves. Mammals sort of just hung reptilian forms. One line retained a skull
around for the next couple of hundred structure much like that of the amphib-
million years until they became more ians from which they had only recently
prevalent after the great extinction of 65 been derived. This line also possessed a
million years ago (mya). Several pri- simple, sprawling form of quadrupedal
marily aquatic forms evolved from the locomotion powered by legs that were
stem reptiles. Two of these were large, only about 50 million years removed
carnivorous types that are now extinct. from being fleshy fins on lobe-finned
Another included the various types of fishes. Although this form of locomo-
chapter 1

turtles, which have not changed greatly tion can be considered primitive, and it
in the last 180 million years. puts some limits on the size and flexi-
For our purposes, the most import- bility of movement of animals using it,

1stPages_A.indd 4 7/22/20 10:30 AM

 the relatively small lizards and snakes large, amphibious sauropods, and some
that were derived from these forms are ostrichlike dinosaurs.
still with us in great numbers. Despite While everyone agrees that birds
possessing what we consider primitive developed through the thecodont line
structural design, these forms have been of reptiles, there seem to be several
successful in their ecological roles for possibilities for when and where the
250 million years with little change. avian line separated from the reptilian
The other major radiation of (fig. 1.1), or if such even occurred. The
land-dwelling reptiles was first char- flying reptiles (pterosaurs) might seem
acterized by a newer, more effective a logical choice for avian ancestors, but
form of locomotion. The most apparent the differences between the pterosaur
change here was a tendency to increase wing and the bird wing are so extreme
the size of the hind legs and shift them that no way can be seen to get from one
so they were situated below the body. to the other. Certainly, the membranous
Initially, this allowed short bursts of pterosaur wing was an alternate means
bipedal motion from a quadrupedal of gliding and flying; pterosaurs were
lizard, a behavior that we see in some successful during most of the Age of
lizards today. With greater development Reptiles and ranged in size from spar-
of the hind legs, though, forms evolved rowlike to those with 27-foot wingspans.
that were totally bipedal. Many varieties were carnivores, often
In addition to providing greater specializing on fish, while the largest
agility and speed of locomotion, the may have scavenged dead dinosaurs.
evolution of bipedalism effectively freed All the pterosaurs disappeared at the
the front limbs for other activities. The end of the Cretaceous with the rest of
line of mobile reptiles evolving in this the dinosaurs. Another alternative for
fashion was called the thecodonts (fig. the evolution of birds is that they split
1.1). Early thecodonts had smaller front from a crocodilian ancestor sometime
legs (suggesting only some bipedalism), during the early radiation of the archo-
conical teeth set into deep sockets, and saurs. Birds and crocodiles share almost
a variety of skeletal shifts to support identical inner ear structure, several
this new body plan. The thecodonts are sets of bones that are very similar to
considered the ancestors to the full line one another but differ from those of
of archosaurs that dominated during the other existing vertebrates, and aspects
Age of Reptiles, a period of nearly 150 of parental care that are rare in other
An Introduction to Ornithology

million years. This group included the current reptiles. Several scientists have
crocodiles, the flying and gliding ptero- made detailed studies of the similarities
saurs, and the dinosaurs. The dinosaur of these forms, but support for this idea
line split rather quickly into two groups, has declined as evidence in favor of one
the Ornithischia (dinosaurs that had of the other models has advanced. In
birdlike pelvises but were not further particular, the behavioral similarities
associated with bird evolution) and the are not that special, as over 100 spe-
Saurischia (dinosaurs with reptilian cies of snakes and lizards show some
pelvises). The latter group included car- form of brooding behavior for eggs or
nivores such as Tyrannosaurus rex, the nests. Thus, most look elsewhere in

1stPages_A.indd 5 7/22/20 10:30 AM

 Fig. 1.2. How a fossil Archaeopteryx may have
Archaeopteryx
looked upon its discovery.

It has been only about 150 years since

the thecodont line for the avian ances- workers in a limestone quarry in Ger-
tor. Before we examine the two most many uncovered a peculiar fossil (fig.
popular theories available, let us jump 1.2). The rock formation in which they
ahead and look at the next generally were working was believed to date from
recognized fact, that Archaeopteryx is the the Jurassic, about 130 million years ago.
chapter 1

oldest-known bird. Although the bone structure of this fossil

(including teeth in sockets) was similar
to that of many of the smallest dinosaurs
found in the same deposits, this animal
6

1stPages_A.indd 6 7/22/20 10:30 AM

 had a distinct covering of feathers. The Fig. 1.3. Our interpretation of how
specimen was given the genus name Archaeopteryx may have looked when alive.
Archaeopteryx, meaning “ancient wing,”
and the species designation lithographia, and archosaurs. The bone structure
since the limestone was being mined differs from the reptilian only in the
for use in lithographic printing. It is our presence of a furcula, also known as the
good fortune that a few of these primi- wishbone. In fact, several of the Archae-
An Introduction to Ornithology

tive birds were preserved in these fine opteryx fossils were initially misiden-
limestone sediments, for without them tified as dinosaurs because scientists
the picture of avian evolution would be did not look closely enough to see the
even more confusing. As it is, fewer than sometimes vague imprint of feathers.
a dozen specimens that everyone seems In addition to teeth, Archaeopteryx had
to agree are Archaeopteryx have ever been a long, bony tail, a small sternum, and
found. wing bones unlike those of modern
Although the covering of feathers birds. This structure suggests to some
suggests that Archaeopteryx was a bird that it was a glider but not really devel-
(fig. 1.3), it is in fact almost a perfect oped for powered flight, although others
intermediate between modern birds disagree. Even though there was a long
7

1stPages_A.indd 7 7/22/20 10:31 AM

 way to go from Archaeopteryx to mod- some of the discussion has degenerated
ern birds, we know that at least by 130 into attacks on how different people do
million years ago, birds did exist. science, with mostly older paleontolo-
gists who do things a certain way on one
Theories of Bird Evolution side arguing with younger, nonpaleon-
tologists with new methodologies on the
The evolution of birds in general, and other side. Name calling is sometimes
the evolution of birds from dinosaurs in involved, with one person talking about
particular, attracts a great deal of atten- the other’s “rhetorical sham” or how he
tion from the public. Unlike most of the or she supports an argument with only
topics in this book, the evolution of birds the “sociology of science” rather than
and dinosaurs is a regular subject of data. To get a feel for these arguments,
papers in such upper-level journals as Sci- check out the series of commentaries
ence and Nature, with articles released to and rebuttals by Richard Prum (2002,
local newspapers for general readership. 2003), Alan Feduccia (2002, 2013), and
Everybody loves birds, dinosaurs, or both, Alan Feduccia, Larry Martin, and Sam
and the possibility that birds are dino- Tarsitano (2007).
saurs is almost magical to most people. Much of this discussion occurs
Scientists are also deeply involved because the fossil record is incomplete,
in this controversy about the possible with large anatomical steps between
evolution of birds from dinosaurs, per- existing fossils and millions of years
haps sometimes too deeply. Although with no information. Bird bones are
new fossil discoveries sometimes appear light and hard to preserve as fossils,
that help provide new evidence to fuel which means that feathers are even
the controversy, much of the discus- harder to find. We have already noted
sion revolves around a small number that several of the Archaeopteryx speci-
of fossils that have been analyzed and mens were misclassified until someone
reanalyzed over decades by different looked closely enough to see feather
scientists, with one person convinced impressions. Avian scientists are search-
that a new discovery is important while ing for their own “missing link,” just as
another strongly disagrees. Some of anthropologists who study the evolution
these comparisons are real, as several of humans are. New fossils that might
of the original Archaeopteryx specimens provide evidence toward these argu-
were classified as dinosaurs until some- ments are of great value. Many of these
one looked closely enough to see the have recently been coming from China,
feather impressions; others are simply where the proper deposits to preserve
individual interpretations. As the two bird skeletons exist. Most fossils are
theories of avian evolution have devel- collected by professional fossil hunters,
oped over the past two decades, the dis- who then sell them to scientists and
cussion has sometimes been less than museums. These collectors are well
scholarly. Rather than a comparison aware of what the paleontologists want
chapter 1

between a theory that has been around to find and how much money such
for 100 years versus one that is relatively a fossil might be worth. A few years
new (but was actually suggested first), ago, one ingenious fossil gatherer put

1stPages_A.indd 8 7/22/20 10:31 AM

 together what appeared to be the perfect colleague of Charles Darwin, declared
missing link, one that would have ended that birds were simply glorified rep-
the arguments about the origin of birds. tiles. In its most basic form, this theory
A renowned national society paid a great suggests that paleontologists’ confu-
deal of money to acquire this fossil. sion of Archaeopteryx with some of the
The society had its own paleontologists small, terrestrial dinosaurs had to mean
examine the fossil but would not let oth- something regarding evolution. Such
ers look at it before the highly publicized similar skeletons as shown by primitive
unveiling of the fossil and a story about birds and coelurosaurian dinosaurs
it in the society’s magazine. Unfortu- had to come from similar ancestors in
nately, the members of this group let relatively recent times. Proponents of
their enthusiasm get the best of them. this theory suggested that these two
Once the fossil was open to viewing, sev- groups split from a common ancestor
eral scientists were able to rather quickly not that long before they could be found
show that it was a fraud concocted by a coexisting on the earth. Examinations
very clever Chinese fossil collector. of many of these theropods and early
The dominant theory until fairly birds seemed to reveal the existence of
recently was the pseudosuchian theco- feathers in a wide variety of forms, both
dont hypothesis. This was developed avian and nonavian. By compiling much
early in the 1900s5,although until it was information, Paul Sereno (1999) devel-
attacked by the alternative proposal, it oped a phylogeny suggesting that the
was not particularly detailed. This theory theropod dinosaurs split from the major
posited that since Archaeopteryx was sauropod dinosaur group and then split
so distinctly different from coexisting into three further groups, including the
animals when it occurred, it had to be coelurosaurs (fig. 1.4). Coelurosaurs
the result of a separation from sister included a variety of bipedal dinosaurs
forms much earlier in its history. It was and birds, and this group may have
suggested that an early thecodont such been where feathers first appeared in
as Euparkeria, which was quadrupedal animals. Further down the line, a split
but tended toward bipedal, provided an divided the tyrannosauroids (including
excellent form to turn into a bird, and everyone’s favorite, Tyrannosaurus rex)
perhaps into other archosaur groups, and a diverse group of forms, one of
including dinosaurs and maybe crocodil- which appeared to have well-developed,
ians. Unfortunately, there is no evidence modern feathers and was considered
An Introduction to Ornithology

linking this and Archaeopteryx for about the birds. Such a phylogeny shows birds
100 million years. easily nestled within such dinosaur sis-
The theropod hypothesis has been ter species as T. rex and Velociraptor, the
developed mostly in the past 40 years, star of the movie Jurassic Park. Feath-
but in some ways it is by far the oldest ers of some form, which we suggested
hypothesis for the evolution of birds. earlier were key in distinguishing birds,
In the 1860s, after looking at a fossil were widely present among these birds
Archaeopteryx and fossils of some of the and their dinosaur relatives, with the
terrestrial coelurosaurian dinosaurs, avian groups distinctive because they
Thomas Huxley (1867), friend and had well-­developed feather structure.

1stPages_A.indd 9 7/22/20 10:31 AM

 Fig. 1.4. One of the hypothesized evolutionary
trees of birds through the coelurosaur dinosaur
group, showing the split between tyrannosaurs
and maniraptors, which led to the branch in
which all bird groups seem to occur. It has
been suggested that all these groups had
some sort of feather-like covering, while well-
developed feathers appear only in the bird
groups, and perhaps one or two of the nonavian
groupings, and the splits in early periods
maniraptors. Modified from Sereno (1999).
are also just suggestions. The theropod
model involves a lot of development in
a much shorter period, as the evolution
Which Theory Is Correct? of birds occurred well past the split
between the two major dinosaur types.
Before we get into the details of the Because most ornithologists are
strengths and weaknesses of these two not paleontologists, the origins of birds
theories, we must remind ourselves have been discussed mostly by paleon-
that both suffer from giant gaps in the tologists and ignored by ornithologists.
fossil record. For the thecodont model, By the year 2000, virtually all paleon-
we have a gap of 90–100 million years tologists believed in the theropod origin
between Archaeopteryx and some fos- of birds. When Richard Prum wrote a
sils that might serve as prototypes for commentary for The Auk, the journal
the developing bird. In contrast, the of the American Ornithological Society,
theropod model is based on a variety of the world’s largest ornithological society,
shared characteristics found in a coex- and titled it “Why Ornithologists Should
isting group of animals from the time of Care about the Theropod Origin of
Archaeopteryx; this information can be Birds,” the intellectual battle was on. In
put together through taxonomic meth- one corner was Prum, a broadly trained
ods to present a proposed relationship ornithologist who became interested
among developing forms as shown in in fossil birds later in his career. In the
figure 1.4, but this relationship is based other corner was Alan Feduccia, a life-
on the results of evolution and shared long avian paleontologist. Here are some
chapter 1

traits. There are no fossils to support the of the factors they discussed in their
splits shown in the figure; rather, clus- original papers and rebuttals:
tering techniques suggest the various

10

1stPages_A.indd 10 7/22/20 10:31 AM

 (a) DIGITS: Most vertebrates have Fig. 1.5. Evolutionary change in which digits
hands or feet with five fingers or ​ are kept in different groups. All vertebrates
toes (digits) at some point in their start with five digits but often reduce the
development (fig. 1.5). Both birds and number to three. Theropods keep the first three
theropods have reduced the num- digits, while birds keep digits II, III, and IV.
ber of functioning digits on their
forearms to three, with two vestigial
digits. It appears that theropods have
kept the first three digits (the thumb
plus the next two fingers, labeled I, are blade-like, which is appropriate
II, and III), while in birds, it appears for vicious carnivores but suggests
that the thumb and little finger have separate lines of evolution for these
become vestigial, such that digits groups.
II, III, and IV remain functioning. (c) FEATHERS: We have already
This is a basic enough difference noted that feathers are diagnostic
that we would not expect it to occur for birds among existing animals.
later in evolution. Thus, the digits Obviously, if feathers were shared
suggest that birds do not share a between birds and theropods, it
basic ancestor with the theropods, would suggest a close lineage. All the
which then favors a thecodont mod- groups shown in figure 1.4 may have
el. Scientists favoring the theropod had some kind of feather-like cover-
model have suggested that some sort ing, but only a few of the nonavian
of frameshift might have occurred to maniraptoran groups had the fully
explain this difference between the developed feathers characteristic of
An Introduction to Ornithology

two groups. Some interesting work all birds. Some have suggested that
on the development of the fingers in Tyrannosaurus rex was feathered,
embryonic ostriches has supported at least when young, but there has
the separation of birds and dinosaurs, been great controversy about whether
but this argument is difficult to test feathers really exist on anything other
because dinosaurs are extinct. than birds. Some have suggested that
(b) TEETH: Bird teeth are very some sort of “dino-fuzz” did occur on
similar in all the old bird families in all the coelurosaurs, but that this was
being peg-like and set in sockets. The not necessarily a feathered covering.
teeth of most theropod dinosaurs As we noted earlier, the chemical

11

1stPages_A.indd 11 7/22/20 10:31 AM

 composition of feathers and scales theropods and primitive birds seem
is almost identical, which makes it quite similar, the controversy over the
difficult to be sure which side is cor- relatedness of these two groups has
rect regarding widespread feathering caused some to take a very detailed
on dinosaurs and its role in showing look at the skulls of these groups. It
relationships with birds. On the other has been suggested that the diapsid
hand, a recent paper seems to show arches in the skull show distinct
pronounced evidence of feathers on patterns of evolution within the birds,
Velociraptor.6 eventually leading to what is called
(d) THE TEMPORAL PARADOX: an avidiapsid arch, which is distinctly
As we noted above, birds and birdlike different from the structure of thero-
theropods were known to coexist at pod skulls.
similar times in history. Unfortunate- (g) EVOLUTION OF FLIGHT:
ly, though, it appears that primitive ­Because flight is so distinctive to
birds such as Archaeopteryx appeared birds, the arguments about avian
earlier in the fossil record than the evolution have to consider the possi-
theropods, in many cases by tens of bilities of flight evolving in these two
millions of years. Obviously, “you alternative models. The thecodont
cannot be your own grandmother,” so theory suggests that early archosaurs
it would be impossible for theropods that climbed trees may have devel-
to evolve into birds if birds already oped the ability to extend their glide
existed. by modifying their front legs into
(e) BEHAVIOR: As we have learned wings; such modifications extended
more about dinosaurs in recent years, eventually to powered flight. Archae-
we have seen that they may have opteryx serves as a good example of
had much more sophisticated forms an early stage of such evolution, as
of social and reproductive behavior there is skepticism about the extent to
than most of the existing snakes and which this species was able to per-
lizards on the planet. Such dinosaur form powered flight rather than just
behavior has been described as very extended gliding. This arboreal theory
avian in nature, which would make for the evolution of flight makes a
sense if the two groups were related. certain amount of sense, and we can
While this relationship between the find snakes, lizards, and mammals
behavior of the two groups makes that glide today. If birds evolved
sense, one worries that as science from running dinosaurs, though, the
considers a bird-dinosaur connection, evolution of flight had to occur from
it assigns avian traits to dinosaurs the ground up, the cursorial theory.
when the evidence for such behavior This theory involves modified front
is sparse. For example, it is not very legs where extended scales or feathers
diagnostic to recognize that over 100 allowed a powerful runner to extend
species of existing snakes and lizards a jump over great distances. With a
chapter 1

show parental care at nests, and some little more modification, these feath-
are even communal (nest in groups). ers could provide a power stroke and,
(f) SKULLS: Although the skulls of eventually, powered flight. Arguments

12

1stPages_A.indd 12 7/22/20 10:31 AM

 in favor of the thecodont model sug- studies locomotion of baby game birds.
gest that the aerodynamics of a curso- These birds hatch as very mobile chicks
rial route to flight were a hurdle too that immediately start moving around
significant to overcome, particularly their environment. They quickly develop
with such strongly bipedal organisms short flight feathers on their wings, and
with heavy back legs. Several recent Dial has done experiments showing how
fossils show primitive birds that had even partial wings can help these small
feathered hind legs, and there is even birds move, including allowing them to
some evidence that Archaeopteryx had climb steep rocks by gathering friction
these legs.7 with their legs because of the flapping of
the small wings (which he calls wing-as-
Another problem with the cursorial sisted incline running). We could rather
theory for the evolution of flight is the easily envision a small, bipedal dinosaur
development of large wings after the that developed small wings for this
front legs had become much reduced in advanced mobility for either catching
size as these creatures became bipedal. prey or avoiding being caught as prey,
How could big front legs become small and the small wings then developing
front legs, and then how could these into something adapted for flight.
tiny front legs become modified into As we noted earlier, recent behavior-
large wings that eventually led to flight? ists have suggested that dinosaurs had
This seems to require a step where a much more sophisticated social behav-
short wing that was not actually used for ior than we generally assign to modern
flight had some value, after which the lizards. Such advanced mating behavior
wing could evolve. But how does a half could easily have resulted in strong sex-
wing or quarter wing develop that serves ual selection, that form of natural selec-
some purpose that could eventually lead tion that favors males (usually) that can
to flight? attract the most mates through a variety
John Ostrum, one of the first to of secondary sexual traits. It has been
push the modern ideas of birds as dino- suggested that early feathers in large
saurs, suggested that some of the early dinosaurs served this purpose, which
theropods developed extended scales on could have resulted in long feathers on
their front legs that they used as swatters the wings and tail that were then used to
for capturing the foot-long dragonflies develop flight.10
and other insects that occurred in those
An Introduction to Ornithology

days. After developing these long, modi- What Is the Truth about
fied scales on their front legs, these ani- Avian Origins?
mals started using them for gliding, and
eventually powered flight. But no fossils In the decade since the Prum/​Feduccia
appear to actually show the developing exchanges, discussion has settled down
stages of these fly swatters.8 somewhat. Paleontologists seem to have
An intriguing and perhaps more universally accepted the birds-as-thero-
reasonable model of how an undevel- pod-dinosaur-relatives model, while the
oped wing could be adaptive has been journal Science suggested in 2010 that
developed by the work of Ken Dial.9 Dial the “bird-dinosaur link [had] firmed up.”

13

1stPages_A.indd 13 7/22/20 10:31 AM

 Fig. 1.6. Our version of a colorful, four-winged
bird that may have occurred early in the
evolution of birds.

1stPages_A.indd 14 7/22/20 10:31 AM

 Numerous exciting fossils have been become biased. It is interesting reading,
found in China over this decade, some no matter which side you favor. Fed-
of them suggesting rather bizarre birds uccia and Stephen Czerkas (2015) also
with full wings on both front and back present intriguing evidence that some of
legs. Paleontologists have made good the large, walking maniraptoran dino-
cases that many of these early birds were saurs that were suggested to be avian
colorful (fig. 1.6), perhaps even with iri- ancestors possessed a propatagium. A
descent (shiny) plumage. These discov- propatagium occurs only in flying birds
eries are almost always presented within or birds that once flew. Their argument
the framework of a theropod model. is that formerly flying birds moved to
Among several recent books on avian the ground, became large and flightless,
evolution, one titled “Glorified Dinosaurs: and acted like terrestrial dinosaurs even
The Origin and Early Evolution of Birds” though they were birds. In a review of
examines the evidence for theropod Feduccia’s book, Walter Bock (2015)
origins of birds with virtually no men- makes a convincing case that we should
tion of thecodonts.11 Another book is keep an open mind about the evolution
titled Living Dinosaurs: The Evolutionary of birds until we have better evidence
History of Modern Birds.12 One can even from the fossil record.
purchase The Field Guide to Dinosaurs,13 On the prodinosaur side, two
although I am not sure how much use major works appeared in late 2014 and
this will get in the field. early 2015.14 A group of 11 of the most
On the other side, a monograph influential avian paleontologists in the
by Frances James and John Pourtless country present material that is highly
(2009) attempts to reconcile the meth- critical of Feduccia and his approach.
odological arguments that were part of They present a great deal of supporting
the Prum/​Feduccia interaction by using material for their decision that “this
cladistical techniques in what they sug- debate has been settled in the minds
gest is a less biased fashion to explore of all but a handful for decades and the
the validity of six different models of majority of the scientific community
avian evolution. Their results support has moved away from arguments over
some of the alternative models as well as the origin of birds and on to other more
they do the theropod models, and they compelling specific questions.” Another
end with the suggestion that “at present, multiauthored review paper relies on
the origin of birds is an open question.” a very broad, integrative approach to
An Introduction to Ornithology

Building in part on the James and understanding the evolution of a variety

Pourtless work, Alan Feduccia wrote Rid- of avian traits, including feathers, flight,
dle of the Feathered Dragons: Hidden Birds reproductive behavior, and pulmonary
of China (2012), and another perspective systems. This suggests that “the transi-
(2013) in ornithology for The Auk. In tion from ground-living to flight-capa-
both, Feduccia makes exceedingly rea- ble theropod dinosaurs now probably
sonable arguments about what we really represents one of the best-documented
do and do not know about the origins major evolutionary transitions in life his-
of birds, with insights on how science tory.” This review provides extensive new
works and how science can sometimes evidence regarding evolution of digits,

15

1stPages_A.indd 15 7/22/20 10:31 AM

 feathers, flight, and other related traits. The Radiation, Extinction, and
Is the debate over? Perhaps. It is Radiation of Modern Birds
hard to go against the material pre-
sented by N. Adam Smith and his ten Rapid evolution of birds occurred during
colleagues or Xing Xu and his six coau- the Age of Reptiles, when dinosaurs
thors regarding the evolution of birds, ruled the earth and mammals simply
but I still personally find it difficult to tried to hang on. While it is believed
give up on the old explanation. That that both the Archaeopteryx and the
may be my bias, as I was raised on the four-winged bird lines went extinct
thecodont model and I tend to be the rather quickly, two major groups of
same age as most of those who support birds evolved into a variety of types
it. Perhaps I have just bought into what during the period from 150 mya to 65
was described as the “rhetorical sham” of mya (fig. 1.7). One of these groups was
support for this model, or my age affects the enantiornithines (known as the
the impact of the “sociology of science” “opposite birds” because the articulation
on me. Most of my graduate students between the scapula and the coracoid
seem to favor the theropod model, was completely the reverse of that found
perhaps for the same reasons I am in modern birds), which developed into
less comfortable with it. If that model birds ranging from sparrow to vulture
is correct, then modern ornithology is sized. Another group is considered the
simply the study of the surviving dino- primitive ornithurines, which includes
saurs. This may be way cool, or perhaps such groups as the Hesperornithiformes
it means that ornithology should be just (heavy-bodied divers), Ichthyorni-
a section of herpetology, dividing time thiformes (tern-like aquatic birds), and
with the snakes, turtles, and lizards. the poorly known Apsaraviformes
I encourage everyone to keep an (Ambiortiformes).16 Little evidence exists
open mind regarding the question of that any of these early forms ended up
avian origins. Other points of view may leading to modern birds, although the
end up being important in figuring out world 66 million years ago appeared to
what really happened. For example, a have a broad diversity of birds.
recent study done by morphologists who A recently discovered new fossil of a
are totally separate from the controversy species named Archaeornithura meeman-
about bird evolution shows that birds nae is estimated to be 130 million years
are “knee runners,” animals that run old.17 This fossil is very similar to mod-
with the thigh bone almost fixed.15 All ern birds and is considered the oldest
other land animals move their thighs example of something that may have
as they run. For birds, knee running is led to modern birds. But few such avian
needed to keep their air sacs functioning fossils exist that are that old, and most
properly, which is necessary for flight. of the first records for modern forms of
For this reason, most physiologists are birds occur at only around 70 mya or
almost certain that birds could not have more recently, although the new species
chapter 1

evolved such an unusual mechanism for suggests that there was a lineage of mod-
breathing unless they separated from ern birds throughout the period from 130
their dinosaur relatives long in the past. mya to the giant change of 65 mya.

16

1stPages_A.indd 16 7/22/20 10:31 AM

 Fig. 1.7. A summary of avian radiation, then
Most know that this Age of Reptiles
extinction, then radiation over the past 150
million years. Note that Archaeopteryx and
ended about 65 mya when an asteroid
its relatives went extinct early in time, while hit Central America, changed the world’s
the enantiornithines and ornithurines became climate, and caused the extinction of
diverse before disappearing during the K-T nearly all the dinosaurs. This piece of
collapse. Some of the ancestors of modern rock was about 10 km in diameter and
birds survived the K-T disaster and have hit the earth at 40 times the speed of
diversified greatly in the past 65 million years. sound, producing an impact equivalent
The recently discovered bird Archaeornithura to 100 trillion tons of TNT. This impact
An Introduction to Ornithology

sits by itself because it is an extremely old fossil resulted in debris being sent high into
but has no clear evolutionary pathway from the atmosphere, with some of it going
the fossil record. halfway to the moon before coming
back because of the earth’s gravitational
pull. The dust from this event, plus an
outbreak of volcanic activity that may or
may not have been related to the aster-
oid, resulted in widespread fires, mas-
sive cloud cover, and a dramatic increase
in the earth’s atmospheric temperatures.

17

1stPages_A.indd 17 7/22/20 10:32 AM

 It is suggested that 75% of the species that most of the evolution of modern
in existence on earth went extinct, but birds can be traced back only about 65
some areas served as refuges for some million years to the relatively few forms
species. that were able to survive through the
This period is known as the Cre- darkness and cold of the postcollision
taceous-Tertiary (K-T) boundary, as it period. Recent work suggests that all
ended one age (Cretaceous) and opened the placental mammals that occur today
another (Tertiary). Although the K-T arose after the K-T boundary, suggesting
boundary is famous for its effects on that most of our birds and mammals are
dinosaurs, recent evidence suggests that of relatively recent origin.
it had tremendous effects on birds too.18 There is considerable controversy
The enantiornithines and primitive about which forms of birds had evolved
ornithurines all disappeared. Some birds before the K-T extinctions, and the
survived, perhaps some ostrich relatives whole idea of massive avian extinctions
and some birds called “transitory shore- at that time is fairly new. As you can
birds,” and it is from these that all mod- see by the references, some of the same
ern birds have evolved. Data suggest that people are involved in this discussion as
an amazing amount of change occurred were involved with the controversy about
during the first 10 million years after the birds and dinosaurs in the earliest evo-
K-T boundary, such that most modern lution of birds. With so much evolution
avian forms except the Passeriformes followed by a great deal of extinction,
appeared within that time. The Pas- we are a long way from clearly following
seriformes started to radiate about 30 the exact path from the first bird to the
million years ago. This model suggests modern birds we see today.
chapter 1

18

1stPages_A.indd 18 7/22/20 10:32 AM

 C HA P T E R 2

General Traits of an
Avian Flying Machine

B
irds are distinctive for their related to flight. High power comes
powers of flight. Although directly from highly developed breast
other animals fly, in no major muscles, which may account for half
group is flight such a dominant of the bird’s body weight in a strong
part of the general lifestyle. Because the flier. Keeping these muscles working
constraints of flight are severe, birds as requires a hot, hard-working engine
a group are relatively uniform in shape (bird body temperatures run from 107°
and overall structure. Even the small to 113°F). Among the adaptations for
number of flightless birds have evolved this are a highly vascularized breast
from flying forms, so they show rela- muscle supported by a four-chambered
tively few deviations from the standard, heart, high blood pressure, and high
aerodynamic design. While we will focus blood sugar levels. A bird’s heart weighs
here on adaptations for flight, remember proportionately six times more than a
that all birds alight and move around on human’s. Oxygen is gathered by a lung
ground, water, or both, so compromises and air sac system that occupies about
must also be struck with terrestrial or 20% of a bird’s volume (compared to 5%
aquatic locomotion. Much of the vari- in humans) and that also provides an
ation in the avian form is related to efficient cooling system. A highly effi-
the proportion of time spent walking cient digestive system converts food into
or swimming versus flying. Yet even energy, but even with high efficiency, the
with this variation, we can rather easily requirements of flight force many birds
visualize a standard version of an avian to specialize on high-energy foods such
flying machine. Before we look at all the as insects and seeds.
components in detail, let’s see how they A lightweight body is achieved by a
must fit together. number of modifications. The skeleton
Building a bird is not unlike build- is strong but light, with many hollow
ing an airplane, a fact not lost on early bones and reduction or fusion of oth-
engineers. The ultimate requirements ers. The bones account for only 4.4% of
for flight are high power, low weight, body weight in a pigeon, compared to
and a balanced yet streamlined design.1 5.6% in a rat. Sex organs become large
A bird is unlike an airplane in that it only when needed; the remainder of
also must carry some structures (such the time they are small and lightweight.
as a reproductive system) that are not The important extremities of wings and

19

1stPages_A.indd 19 7/22/20 10:32 AM

 tail are formed by feathers, which are similar chemical composition.2 Unfor-
among the lightest yet strongest sub- tunately, the development of the feather
stances found in nature. The body is also from the scale is lost in the fossil record
covered with feathers, and their high along with the early development of the
insulation value allows birds to have very bird. Those who favor a cursorial (run-
thin, lightweight skin. ning) origin of birds feel that feathers
Balance and streamlining are the developed before flight, either as insula-
final requirements. Most birds have tion for these early, warm-blooded forms
exchanged powerful jaws and teeth for a of dinosaurs, or as protection from
muscular stomach or gizzard, which can radiation. Only later were they used for
be packed within the body at the center flight. The argument that birds devel-
of gravity. Although the bill still serves oped as gliding, then flying, lizards may
a variety of food-gathering functions, it favor the development of flight feathers
can be lightweight and streamlined for first, with the insulative traits of body
flight. Body feathers serve to contour the feathers arising later. Whatever their
outer surface for smoothness. The feet origins, by the time that Archaeopteryx
are retractable so they do not interfere lived, feathers were well developed, and
with flight, and no external ears are pres- they have continued to cover all birds
ent. All the heavier support structures since that time.
(skeleton, muscles, digestive tract) are Feathers grow out of a follicle in
located near the center of gravity, which the skin. Although highly vascularized
helps balance the bird. during growth, mature feathers are
We will see later some of the various “dead” in the same way that human hair
options available within this general is dead tissue. A typical perfect feather
design. Now, as we look at the compo- has two parts, a main feather plus
nent parts of the “general” bird in detail, an afterfeather (commonly called an
keep in mind how the avian design aftershaft; fig. 2.1). The two parts share
requires that each part be as light as a common base called the calamus that
possible and that it fit within the dimen- is embedded in the follicle, but each has
sions necessary for flight. a separate shaft called the rachis. For
those large feathers that are instrumen-
Shaping the Bird: Feathers and Skin tal in moving air during flight, the vane
Feather development and structure or web grows from the rachis and is
composed of barbs, barbules, and barbi-
The feather is the most distinctive char- cels, some of which (called hamuli) have
acteristic of a bird and certainly one of hooks (fig. 2.2). These hooks interlock
the most important. Feathers form the the barbules to make a feather strong
flight surface and greatly improve flight yet flexible. Without them, as in most
efficiency. They also provide exceptional afterfeathers, the feather is soft and
insulation to the body and help it main- fluffy or downy (termed plumulaceous),
chapter 2

tain high temperatures with minimal particularly if the rachis is also soft. A
heat loss. The feather is a modified feather without an afterfeather is termed
reptilian scale, and these seemingly pennaceous.
different derivatives of the skin have very Many variations of feather structure

20

1stPages_A.indd 20 7/22/20 10:32 AM

 a

b b

c
d

e
g

Fig. 2.1. Different types of contour feathers

found in birds. These include a primary feather
from the wing (a), two body contour feathers
h
(b), a body down feather (c), a body down
feather with an aftershaft (d), a down feather
(e), a powder down feather (f ), a bristle (g),
and a filoplume (h).

1stPages_A.indd 21 7/22/20 10:33 AM

 occur (fig. 2.1). The feathers seen most Fig. 2.2. Complex levels of structure of a
often in adult birds are termed contour feather, from rachis (shaft) to barb, barbules,
feathers. These form the body covering and barbicels, some of which have hamuli that
(often with perfect feathers) and the hook together.
wing and tail (which are usually pen-
naceous feathers). Although contour
feathers are usually normal feathers, These feathers grow continuously at the
this group also includes semiplumes base and disintegrate at the tip. A bird
and bristles. A semiplume often resem- may spread the waxy powder produced
bles an enlarged afterfeather, whereas by this disintegration throughout the
bristles look like hair and may occur plumage to protect it from moisture or
around the mouth (rictal bristles), to help clean it. Such birds usually lack a
nostrils, or eyes (eyelashes). Another uropygial gland.
type of hairlike feather is the filoplume, Although it appears that most birds
although this differs from a bristle by are covered with feathers, only in the
growing in clusters, encircling the base South American screamers and the
of the contour feathers. Down feathers flightless ostriches and penguins do
(plumules) lack a vane and may lack feathers grow generally all over the body
a rachis, such that barbs fan out from surface. In other birds, feathers grow in
the top of the calamus. Down in adults areas called tracts or pterylae (fig. 2.3),
occurs beneath the contour feathers and with bare areas (apteria) between. The
is most pronounced in aquatic birds. study of such tracts is called pterylogra-
Birds such as chickens and ducks have phy and may reveal relationships among
chapter 2

downy young, although this down is species (see chapter 6).

somewhat different from that found on In addition to the apteria, many
adults. Perhaps the most specialized birds have bare areas of skin that are
feather type is the powder down feather. exposed. Most pronounced among these

22

1stPages_A.indd 22 7/22/20 10:33 AM

 a b

Fig. 2.3a and 2.3b. (a) Location of feather

tracts (pterylae) shown from a dorsal view
(top) and ventral view (bottom) of (b) a
Clark’s Nutcracker (Nucifraga columbiana)
(Mewaldt 1958).

ornate feathers to show their sex and

breeding status, and males are the most
ornate in most, but not all, species.
Some feathers are modified so that birds
can use them to make noise, usually
as part of their breeding displays. Such
“aeroelastic flutter” is most pronounced
in hummingbirds, but it occurs in a
variety of species.3 Sandgrouse (family
Pteroclidae) of the Old World deserts
are the vultures, whose bare heads may are famous for having modified feathers
be an adaptation for keeping feathers on their belly. These feathers act like
clean while feeding on dead flesh. This sponges, such that a sandgrouse can fly
General Traits of an Avian Flying Machine
bare skin is sometimes brightly colored to a desert oasis, soak these feathers full
and may be an important part of dis- of water, and then fly back many miles
plays. Ostriches (Struthio camelus) and to its nesting site, where it can give its
other ground dwellers have unfeathered babies a drink. Perhaps the strangest
legs that can be used for cooling after variation in feather color is the sugges-
heavy exercise. At the other extreme, tion that feathers on some individuals
Arctic species often have legs and feet of the Barn Owl (Tyto alba) are biolumi-
that are feathered to preserve heat. nescent, which means they glow in the
Although the purpose of most dark.4 It is not known how widespread
feathers is related to either flight or this phenomenon is.
insulation, some species of birds have
modified their feathers for other pur-
poses. Males of many species use very

23

1stPages_A.indd 23 7/22/20 10:34 AM

 Fig. 2.4. Molt of a typical male songbird annual molt when environmental condi-
(Bobolink, Dolichonyx oryzivorus, left) and tions are severe. Usually wing, tail, and
a male dabbling duck (right), showing cyclic body feathers are molted a few feathers
patterns through life. Molting periods are at a time, but some species (such as
shown in red, nonbreeding plumages in purple, ducks) lose all their wing feathers at
and breeding plumages in blue. Flight feathers once and thus are flightless for a time.
are molted only during the postbreeding
In some species, one of the annual
period (July–August). In both species, females
molts may include all the feathers,
undergo a full molt only once, after breeding
while the second molt includes only the
(Weller 1976).
contour feathers of the head, body, and
sometimes tail.
Molt With so much variation within and
among species in the timing and char-
Although feathers are among the stron- acteristics of molt, it is not surprising
gest materials for their weight found in that several systems of nomenclature
nature, they do wear out. They may also concerning the molting process exist.
support lice that damage the feather Once they achieve adulthood, most
over time. Thus, in addition to being birds (particularly those of the temper-
able to replace individual feathers lost ate zone) fall into a cycle of one or two
by accident, a bird periodically replaces yearly molts and one or two plumage
the whole set by undergoing a process types (fig. 2.4). Often, males undergo
known as molt. The frequency of molts two molts while females do just one.
varies depending on seasonal variation Following one system of nomenclature,
in outward appearance (called plumage) the plumage shown by males during the
chapter 2

and factors related to wear of the feath- breeding season (often the most colorful
ers. An annual molt is most common, plumage) is termed the nuptial plum-
but some species molt several times a age. These feathers are usually replaced
year, and others may omit a complete through a postnuptial molt. If the

24

1stPages_A.indd 24 7/22/20 10:35 AM

 plumage following this molt is different in the cycle, it is the alternate plumage,
from the nuptial plumage, it is termed and the sequence through the cycle
the winter plumage. Usually, this is a consists of basic plumage, prealternate
dull, cryptic plumage, which in some molt, alternate plumage, prebasic molt,
cases is due to dull-colored feather tips and basic plumage. There is no corre-
that simply wear off to reveal the nup- spondence between basic plumage and
tial plumage without a second molt. In nuptial plumage that is consistent from
other cases, a prenuptial molt replaces species to species, so some species breed
the winter plumage with the nuptial in basic plumage and others in alternate
plumage. The prenuptial molt often plumage. This system has the advan-
includes only the head and body feath- tage of clear definitions of plumages
ers, while the postnuptial molt includes and molts that can apply to all species,
all ­feathers. particularly those that live where “win-
Many variations on these themes ter” is nonexistent and breeding cycles
occur. Male ducks are distinctive in may not conform to annual cycles. In a
having a postnuptial body molt that few species, a third plumage occurs; this
results in what is called the eclipse is called a supplemental plumage, and
plumage (fig. 2.4). This usually cryptic it may occur following either basic or
plumage aids the duck in hiding while it alternate plumages. There is still a great
undergoes a flightless period associated deal of discussion and confusion about
with the molt of its wing feathers. Soon the terminology of molts and plumages.5
after the flight feathers are replaced, Young birds go through their own
ducks undergo a prenuptial molt and series of molts before attaining the
attain their nuptial plumage. Hence, the cycles of adults. Most start with a natal
so-called winter plumage in ducks may plumage followed by a juvenile plum-
occur only in July and August. age (or plumages) before reaching the
Because the terminology of nup-
tial and winter plumages is not really Fig. 2.5. Occurrence of black wing tips in white
accurate for ducks and many other and pink birds. View of the top of the wing
birds, a different nomenclature has been is above the bottom view. Species are (from
left) American White Pelican (Pelecanus
developed. In this system, birds with
General Traits of an Avian Flying Machine
erythrorhynchus), White Ibis (Eudocimus
one plumage through a breeding cycle
albus), Caribbean Flamingo (Phoenicopterus
(usually a year) are said to have a basic ruber), and Northern Gannet (Morus
plumage. If a second plumage occurs bassanus).

25

1stPages_A.indd 25 7/22/20 10:35 AM

 adult cycle. Some birds attain an adult A great many factors appear to be at
plumage after only a few months, while work in determining the colors found
others take much longer. A Bald Eagle in each species. Some of these may be
(Haliaeetus leucocephalus) requires five related to structural problems associated
years to attain the full adult plumage, with color formation; apparently certain
and even some small species like the colors help make stronger feathers and
Painted Bunting (Passerina ciris) and thus may be used in areas with higher
American Redstart (Setophaga ruti- wear. This may explain the black wing
cilla) may take two years for males to tips of many white birds (fig. 2.5), as
attain adult plumage. Some tropical black feathers tend to wear more slowly
species with exceptional male plum- than white. Some colors may be selected
age take many years to achieve the full for physiological reasons, either to
male plumage. For example, males of absorb light (dark colors) or to reflect it
the Long-tailed Manakin (Chiroxiphia (pale colors). Colors may aid conceal-
linearis) are five years old before attain- ment of a bird, either by making the
ing the final adult plumage, with slight bird cryptic so that it can blend into its
differences in plumage occurring each environment or by showing a disrup-
year.6 tive pattern such that the bird’s form is
less apparent to a predator. Signaling by
Feather color color is very important in such activities
as species recognition, sexual behavior,
Discussion of nuptial plumage brings flock movements, and warning displays.
up one of the most aesthetically pleas- With so many factors at work it is hard to
ing of avian traits: feather color. Birds explain the occurrence of any particular
display virtually every color imaginable, color in any particular place. By compar-
as a result of the structure of the feather ing species that are sexually dimorphic
itself, pigments within the feather, or (also called dichromatic) in plumage
reflective properties of the feather. These (where the male and female do not look
pigments may be synthesized by the alike), we can get clues to the relative
bird or derived from the diet. For exam- strengths of such factors as sexual attrac-
ple, flamingos get their pink color from tion, aggression, and predator avoidance
carotene in shrimp and will become in determining plumage traits. Eco-
white if not given carotene. No blue pig- logical or behavioral factors that affect
ment exists, and most green birds have plumage will be discussed in several later
no green pigment. Rather, the feather is chapters. Although it is generally felt
constructed in layers such that one layer that we can explain why a male Northern
reflects the wavelength of light that gives Cardinal (Cardinalis cardinalis) is brightly
the color we see while a deeper layer colored while its mate is dull, we cannot
absorbs the other wavelengths. The bio- yet explain why the male is red rather
chemistry and structural modifications than yellow, orange, or bright blue.
chapter 2

involved in producing the spectacularly The role of color variation in birds

iridescent plumages of such species as has been made a bit more confusing by
hummingbirds are exceedingly complex the discovery that birds see a broader
and not totally understood. range of light wavelengths than humans

26

1stPages_A.indd 26 7/22/20 10:35 AM

 do. Thus, birds can see in both lower Fig. 2.6. Variation in light wavelengths seen by
wavelengths (infrared) and higher wave- humans (top) and birds (bottom), and how
this might translate into what a Crested Mynah
lengths (ultraviolet; fig. 2.6). As a result,
(Acridotheres cristatellus) looks like to us (top)
some species have sexes that differ in
versus what it may look like to another bird
color with wavelengths that humans (Street prophets coffee hour 2013).
cannot see. Thus, we think the species is
monomorphic (sexes look alike), when
in truth the male may have spectacular feathers contain a neurotoxic alkaloid
colors on its body that make it quite that makes the birds distasteful to most
clear that it is a male to other birds; we predators. The chemicals certainly
just cannot see it. Several interesting protect the birds from parasites on the
studies in recent years have measured feathers and skin but may also reduce
the wavelengths of light reflected off the birds’ value to predators. The birds
General Traits of an Avian Flying Machine
feathers to assess what color that portion do not produce the alkaloids themselves
of the bird shows to those organisms but get them from beetles in their diet.
able to see those wavelengths. In a few The colors of the Pitohui are remarkably
cases, sets of species that look alike to similar to those of the Monarch Butterfly
humans turn out to be of very different (Danaus plexippus), which is a famously
colors when the type and amount of distasteful insect that gets its repellent
reflectance are measured. chemicals from its diet.
A novel and perhaps rare adaptation
of feathers is found in the genus Pitohui Skin
of the family Pachycephalidae (fig. 2.7).
The six species of this group are found The fact that feathers provide shape
only in New Guinea. They are brightly to the bird, insulate it from the ele-
colored orange-and-black birds whose ments, and may even provide their own

27

1stPages_A.indd 27 7/22/20 10:35 AM

 the rhamphotheca). This is as variable
in size and shape as the beak itself (see
chapter 4), and it may serve a role in sex-
ual signaling or other communication by
being brightly colored or having various
projections. In many species, the beak
may be colored to reduce glare, much as
football players blacken their cheeks. In
some species, the rhamphotheca is very
hard, while in others (sandpipers, ducks)
it may be softer and somewhat flexible.
Recent work has suggested that the beak
may be very important in cooling birds
that live in hot environments.
Another modification of the skin
includes the scales and claws on the feet
of birds. This region (termed the podoth-
eca) results from a change from feathers

l­ubrication reduces the duties of the

skin itself. This makes the skin no less
important, for feathers are outgrowths of
the skin, and an external layer is needed
to cover the organs as well as provide a
barrier to the entry of bacteria and other
microorganisms. The result is a thin,
light, flexible skin. It is attached to the
body at relatively few points to provide
maximum flexibility, and it is unusual in
being directly attached to bone in several
locations (skull and beak, wing tips,
etc.). It contains no sweat glands, and
the oil that some species use to clean
and waterproof the feathers is provided
by a single sebaceous gland (the uropy-
gial gland), located at the upper base of
the tail. Although this is the major skin
gland, the skin itself does secrete small
Fig. 2.7. A Hooded Pitohui (Pitohui dichrous)
quantities of some substances.
apparently has distasteful feathers that serve
Several modifications of the skin are
to protect the bird from predators, in much the
chapter 2

important to birds. Although the foun- same manner as chemicals in the Monarch
dation of the beak is part of the skull, the Butterfly (Danaus plexippus) are protective.
outer surface and parts of the inner beak Both species share a distinctive orange-and-
are covered with modified skin (called black warning coloration.

28

1stPages_A.indd 28 7/22/20 10:38 AM

 on the leg region to scales; the scales in avian form, most of the names of the
terminate on the toe tip with a claw. The areas are consistent from bird to bird.
exact location of the shift from feathers In addition to covering parts of the
to scales varies greatly among birds, with body while at rest, the flight feathers
some Arctic species feathered virtually to provide the propulsion and guidance
the claws. The underside of the podoth- systems of flight. The wing feathers, or
eca is composed of thick pads, usually remiges (fig. 2.9), are composed of (1)
with tiny, modified scales. The size and the primaries, which range in number
shape of these pads depend primarily from 9 to 12 in flying birds and are
on how terrestrial a bird is, while in attached to the bones that correspond to
aquatic species the podotheca may show the hand in humans; (2) the secondar-
some form of webbing. Claws or nails ies, which range in number from 6 to 32
are found in all species but vary from and are attached to the ulna (a forearm
vestigial on some of the toes of ostriches bone); (3) alula feathers (usually 2 to 6),
to long and sharp on birds of prey. which are attached to the thumb; and (4)
A final set of skin modifications is sometimes a few tertials attached to the
associated with sexual and/​or domi- humerus. The number of flight feathers
nance signaling within a species. These is higher in more-primitive flying birds
ornaments include the often brightly than in modern species. The wing and
colored wattles or combs of chickens flight feathers are contoured by the vari-
and chicken-like birds, the air sacs of the ous sets of wing coverts.
neck and throat associated with some The tail feathers, or rectrices, aid in
avian displays, and the brightly colored stabilization and maneuverability. There
bare areas around the eyes of some trop- are usually six pairs of tail feathers,
ical species. although the number varies from 6 to
32. The rectrices are covered at the base
Shape and form by tail coverts. The length and shape of
the tail are usually related to the type of
As mentioned earlier, our “flying flight used by the species (see chapter
machine” must be shaped so that the 3), but some birds have unusually long
center of gravity and the propulsion sys- tails that are apparently used as sexual
General Traits of an Avian Flying Machine
tem are properly balanced. This is done display signals.
by making the body compact and placing As you can see, the feather is an
all the heavy organs near one another at exceptional adaptation to the unusual
the center of the body, yet including an requirements of flight. It is light yet
outer layer of contour feathers to smooth strong; it can be long and thin to propel
the surface and aid the streamlining of a bird, short and rounded to provide a
the body. Figure 2.8 shows the external smooth outer surface, or short and soft
appearance of a typical bird with the to provide insulation. How many feath-
various topographic features labeled. ers does it take to do all this? Not every
This bird is for schematic purposes only, species has been checked, but counts
as all these features are generally not range from 940 feathers on certain
present on a single bird. Although we hummingbirds to 25,216 on a Tundra
will later point out the many variations Swan (Cygnus columbianus).

29

1stPages_A.indd 29 7/22/20 10:38 AM

 Fig. 2.8. Names of the parts of a bird at rest. of the fragility of the skeleton result-
ing from decreased bone density (fig.
2.11). The pectoral girdle is fused to
a great extent in birds, with the large
The Skeleton coracoid bracing the shoulder from the
sternum. Together with the smaller
While feathers do an exceptional job scapula and furcula, the coracoid forms
as an external covering and support a strong tripod of bone in the shoulder
for flight, support within the body is that prevents it from being drawn into
provided by the skeleton. Here again, a the sternum when the powerful flight
balance must be struck between require- muscles contract. The thoracic verte-
ments of strength, support, and flexibil- brae are fused and provide resistance to
ity, and the need to keep the bird as light the contraction of the ventrally located
as possible. Many of the larger bones and flight muscles. They articulate with the
the bones of the skull are hollow, with V-shaped ribs, which in turn articulate
chapter 2

reinforcing struts that provide excep- with the sternum. The last thoracic, all
tional strength with little weight (fig. of the sacral, and six of the caudal verte-
2.10). brae are fused into a synsacrum, which
Fusion of bones overcomes some joins the inner walls of the pelvic girdle

30

1stPages_A.indd 30 7/22/20 10:38 AM

 Fig. 2.9. Names of the parts of the wing, tion of the tarsal and metatarsal bones
showing how they attach to the bones. of the foot give rise to the tarsometatar-
sus, or apparent lower leg, of the bird.
and helps stabilize the pelvis for landing From this bone extend the four digits on
and walking. The terminal vertebra, the which the bird walks.
pygostyle, is the result of the fusion of Despite the reduction and fusion of
several caudal vertebrae and serves as its elements, the bird skeleton is very
a broad base for the attachment of the flexible. Birds have more cervical verte-
rectrices. The 2nd, 3rd, and 4th meta- brae than mammals, and the number
carpals differ from those in mammals varies from species to species. As the
in that they are fused into an elongated only vertebrae that are not fused, they
carpometacarpus in the wing and serve provide the flexibility for the bird to
as the attachment sites of the primary move its head (the chief food-gathering
feathers (fig. 2.9). Fusion and elonga- apparatus) in all directions. In addition,

Fig. 2.10. Examples of hollowness in large

wing bones (left) and the avian skull.
Struts provide extra strength without
sacrificing weight.

31

1stPages_A.indd 31 7/22/20 10:39 AM

 a
Fig. 2.11a and 2.11b. (a) (at left) Names of all
the bones of a chicken, and (b) (following
page) a comparison of the legs and arms/​
wings of a bird and a human (Lucas and
Stettenheim 1972).

1stPages_A.indd 32 7/22/20 10:40 AM

 b

the first cervical vertebra, the atlas, has circulatory, respiratory, and excretory
only one contact point with the skull (at organ systems that provide power to the
the occipital condyle), and this permits muscles to move the bird around.
greater rotation of the bird’s head on
its neck than is possible in mammals. Digestion
Perhaps you have marveled at the ability
of owls, which seem to have no neck at As in most animals, the avian digestive
all, to turn their head more than 180°. system is a tube, with various adapta-
Another type of bone found in birds tions in structure and function as food
is medullary bone. This forms within progresses through the tube. The bill is
the marrow of larger bones and seems the point of entrance into the digestive
to function as a storage site for calcium. system. In chapter 4, we will examine
When birds are laying eggs, this bone the variety of bill types and their utility
General Traits of an Avian Flying Machine
provides calcium that is converted to in birds. The bill may act as an append-
eggshell. age and is critical in capturing prey,
ripping or crushing it into small pieces,
The Avian Propulsion System or filtering out nonedible materials.
The tongue may also be important in
So far, we have constructed only a set handling food. Many nectar-eating birds
of feathers and skin wrapped around have tubular or brush-tipped tongues
a lightweight skeleton. To make this a for lapping up nectar; woodpeckers have
functional flying machine we need an extremely long tongues with barbed
engine and a drive train. In this case tips that can be extended deep into tree
the drive train is the musculature that crevices to capture grubs or other such
manipulates the bones and feathers, food. Filter feeders such as flamingos or
and the engine is the set of digestive, shovelers (ducks) have complex adapta-

33

1stPages_A.indd 33 7/22/20 10:40 AM

 tions to the bill and to the size and shape secrete an amylase enzyme that initiates
of the tongue that allow these often large the chemical breakdown of starch. Taste
birds to exist on microorganisms that buds are found on the tongue but are
they can eat efficiently because of these far less numerous than those of mam-
modifications (fig. 2.12). For most small mals (see the discussion of sense organs
birds, though, the tongue is not particu- below).
larly large or distinctive. After food is swallowed it passes into
Once the food has been handled the esophagus, a simple tube that trans-
by the beak ​or tongue, it enters the oral ports materials from the food-gathering
(buccal) cavity and is then swallowed. apparatus of the head to the food-pro-
Generally, food spends little time in the cessing parts of the body (fig. 2.13). As
oral cavity, but some species have saclike we pointed out earlier, these latter parts
diverticula associated with either the oral are situated at the center of the body to
cavity or upper esophagus. These may
be used for carrying or storing food in
Rosy Finches (Leucosticte arctoa) and Pine Fig. 2.12. Examples of variation in the structure
of the avian tongue, showing the brushy-
Grosbeaks (Pinicola enucleator) or may
tipped tongue of the nectar-thief Bananaquit
be inflated with air during the breeding
(Coereba flaveola); the long, fleshy tongue
display of male bustards. These sacs
of a Red-headed Woodpecker (Melanerpes
usually lie ventral to the jaw and tongue erythrocephalus), with a barbed tip for catching
apparatus, so that their filling does not grubs in wood; the complex filtering mechanisms
interfere with feeding or swallowing. Sal- of the Northern Shoveler (Anas clypeata), which
ivary glands are distributed in the walls sieves microorganisms from the water, and the
of the oral cavity; they not only lubricate fairly typical tongue of a generalist American
the food for ease of swallowing but also Robin (Turdus migratorius).
chapter 2

34

1stPages_A.indd 34 7/22/20 10:40 AM

 aid the aerodynamic balance of the bird. is the metabolic warehouse that converts
Along the length of the esophagus may absorbed nutrients into sugars and fats
be one or a pair of enlarged pouches for for storage, synthesizes the proteins that
food storage called the crop. The size of circulate in the plasma, and catabolizes
the crop varies from a slight swelling of hemoglobin, hormones, and proteins
the esophagus to large diverticula (sacs) as well as other foreign molecules (e.g.,
off the esophagus. Most often the crop drugs, toxins, etc.) for excretion by
is used for food storage, particularly in the kidneys. In addition, it produces
granivorous species, and can expand to a bile that emulsifies fat droplets in the
large volume, filling the often-empty space intestine so that lipases secreted by the
by the furcula. A distensible food-storage pancreas can chemically break down the
organ like the crop enables birds to eat a fat. The pancreas secretes large quan-
lot of food quickly and then digest it in tities of bicarbonate into the intestine
another location, thereby reducing their to neutralize the acid produced by the
exposure to predators. By packing the crop stomach, as well as a large number of
full of food at dusk, diurnal birds can pass digestive enzymes (amylases, proteases,
food into the digestive system for the first lipases) that aid chemical breakdown of
few hours after dark, thereby reducing the food in the intestine. The pancreas is
period of overnight fasting. also essential in the control of sugar and
The esophagus terminates in the stom- fatty acid levels in the blood, achieving
ach, which in birds may be divided into this with the secretion of two antago-
two sections. The more anterior, glandular nistic hormones, insulin and glucagon
stomach contains mucous and digestive (see the discussion of endocrine glands
glands that secrete protease enzymes and below). Both these organs are relatively
hydrochloric acid to chemically break down large in birds compared to mammals.
food. The more posterior, muscular stom- The jejunum and ileum of birds are
ach (gizzard) possesses two pairs of oppos- not as easily separated as in mammals;
ing muscles: thin muscles (or cheeks) and they are greatly coiled and fill the lower
thick muscles (or jaws). The latter muscles part of the abdomen. At the junction
physically grind the food into small parti- of the ileum and the large intestine
cles much as the teeth and jaws of a mam- (also called the colon or rectum), single
General Traits of an Avian Flying Machine
mal would. The grinding that occurs in the or paired lateral pouches called ceca
muscular stomach also aids the mixing of (singular, cecum) may be present. The
food with digestive enzymes. In some spe- primary function of these pouches is
cies, the grinding efforts are aided by grit, microbial fermentation, but recent evi-
which the bird ingests along with its food. dence indicates that the ceca play a role
Once the food has been mechanically in water and electrolyte balance as well.
and chemically broken down, it enters The colon extends from the ileocecal
the small intestine for final processing junction to the cloaca and is relatively
and absorption. Secretions from the liver short in most species. It is another
(bile) and pancreas (digestive enzymes) important site of water and electrolyte
enter the first section of intestine, the reabsorption. In some species, the colon
U-shaped duodenum. These organs also exhibits an unusual property of reverse
have important roles in digestion: the liver or antiperistalsis, that is, movement of

35

1stPages_A.indd 35 7/22/20 10:40 AM

 intestinal contents from the cloaca up crop is 50 times larger than most crops,
the tract toward the ileocecal junction. but it replaces some of the other organs
Antiperistalsis also occurs in the small lower in the digestive tract. In many
intestine, when intermittent strong fish-eating species, the salivary glands
contractions sweep duodenal contents may be completely absent. The esopha-
back into the muscular stomach. This gus has been modified in many species
refluxing of intestinal contents occurs in to serve a secondary role in nutrition of
response to acid, protein fragments, or the young. In pigeons, the crop secretes
high fat content in the duodenum and “pigeon’s milk,” which is rich in fat and
slows the passage of digesta from the protein but devoid of carbohydrates and
muscular stomach. calcium, unlike mammalian milk. The
The colon empties into the cloaca at esophagus of both sexes of the Greater
the coprodeum; urinary waste and repro- Flamingo (Phoenicopterus ruber) pro-
ductive products enter the cloaca at the duces a red juice that is regurgitated for
urodeum. The posterior portion of the the young. Similarly, the esophagus of
cloaca, the proctodeum, stores the mate- the male Emperor Penguin (Aptenodytes
rial from the more anterior regions until forsteri) produces a high-fat, high-protein
a defecation reflex occurs, which moves fluid that is fed to the newly hatched
it out the external opening, or vent. In chick until the female returns from feed-
young birds, a dorsal projection of the ing at sea.
urodeum called the bursa of Fabricius In species with softer diets, the
is present. This lymphoid organ aids muscular stomach is relatively small
in antibody production in juveniles but and in some cases may be bypassed (fig.
disappears at sexual maturation. 2.13). For example, in flowerpeckers and
There is a great deal of variation honeyeaters that feed primarily on soft
in digestive system anatomy, primarily fruits, the muscular stomach is a side
because of variation in diet (fig. 2.13). pouch of the digestive tract. Soft fruits
Birds that have hard, dry diets (such as pass through the tract without entering
seeds) often have numerous salivary the gizzard, while harder foods such
glands in the mouth, esophagus, or crop as insects enter the muscular stomach.
whose secretions aid the passage of food In contrast, the muscular stomach of
into the stomach. Species that include gallinaceous birds (e.g., chickens) is
leaves in their diet often have large ceca, extremely well developed and is the
which serve as a second site for break- primary repository of the food before it
down of plant material. After some time enters the intestine. In carnivores, the
in the ceca, the material moves back into muscular stomach may collect the indi-
the intestine so that nutrients can enter gestible parts of the prey (teeth, bones,
the bloodstream. The ultimate system fur, etc.) and is responsible for com-
to handle a diet of leaves is found in the pacting them into a pellet that can be
Hoatzin (Opisthocomus hoatzin), a tropi- regurgitated. Pellet formation and regur-
chapter 2

cal bird whose diet is composed solely of gitation occurs in owls, hawks, gulls,
leaves. It digests these leaves in a mod- goatsuckers, swifts, grouse, and many
ified crop, where foregut rumination passerine species as well. The size of the
such as that found in cows occurs. This muscular stomach may also vary annu-

36

1stPages_A.indd 36 7/22/20 10:40 AM

 Fig. 2.13. Examples of variation in the structure its intestinal tract before it can success-
of the intestinal tracts of birds, showing, fully eat and digest food.
from the left, a Red-tailed Hawk (Buteo The lengths of the intestine and
jamaicensis), a Hoatzin (Opisthocomus intestinal ceca are also variable among
hoatzin), a partridge (Perdix), and a birds (fig. 2.13). In general, the intes-
hummingbird. The upper esophagus and crop tines tend to be shorter in frugivores,
are shown in beige, the lower esophagus and
carnivores, and insectivores and longer
glandular stomach are in purple, the muscular
in granivores, herbivores, and pisciv-
General Traits of an Avian Flying Machine
stomach (gizzard) is shown in cross-hatched
ores. For example, the intestinal length
purple, the small intestine is in green, the
cecum (or ceca) is shown in pink, and the large of the Common Swift (Apus apus) is
intestine/​cloaca is in blue. roughly 3 times the body length, com-
pared to more than 20 times the body
length in the Ostrich (Struthio camelus).
ally in species that eat insects in sum- Long ceca are found in species such as
mer but seeds in winter. Recent studies ducks, geese, cranes, ostriches, and most
have shown that some shorebirds that gallinaceous birds that eat green plant
migrate extremely long distances can matter or other diets high in cellulose.
absorb much of their intestinal tract In grouse the ceca may be as long as the
before leaving, converting it to fat for intestines, while in some insectivorous
use while migrating. Upon arrival after songbirds, the ceca are very small or
a long flight, the bird must then rebuild even lacking.

37

1stPages_A.indd 37 7/22/20 10:41 AM

 Respiration which increases the efficiency of gas
exchange.
The digestive system converts food into Let’s look at this complex system
a form that can be utilized for energy, of air movement in more detail (fig.
but this process requires oxygen and 2.14). Air entering the nostrils or open
produces carbon dioxide as a waste prod- bill passes through the mouth and
uct. Provisioning the tissue with oxygen through a small slit in the floor of the
and removing the carbon dioxide is the mouth (the glottis) into the trachea. The
primary job of the avian respiratory sys- larynx, found at the most anterior end
tem; this system also aids in producing of the trachea, is a cartilaginous struc-
sound and in cooling the hard-running ture with many ligaments and muscle
avian engine. attachments. It prevents entry of foreign
The most important difference bodies into the airway and can also mod-
between the avian and mammalian ulate the sounds emanating from the
respiratory systems is that birds exhibit syrinx, located farther down the trachea,
a unidirectional flow of air through the by altering airway resistance. Unlike the
lungs during both inspiration and expi- mammalian analogue, the avian larynx
ration. The blind-ending alveolar sacs
of mammals are replaced by an anasto-
mosing network of parabronchi and air Fig. 2.14. Breathing patterns in a bird. Air
involved in the first inhalation moves to
capillaries. Rather than a tidal flow of air
the posterior air sacs (purple); on the first
in and out of the blind-ending bronchial
exhalation, this air moves to the lungs. On
tree as in mammals, birds have a bel-
the second inhalation, old air moves from the
lows-like system of air sacs that provides lungs to the anterior air sacs, while new air
a continuous flow of air through the (red) moves to the posterior air sacs. On the
lung. In addition, unlike in the mamma- second exhalation, the first batch of air (olive)
lian bronchial tree, there is no dead air is expelled, while the second breath moves to
space in the lungs and air sacs of birds, the lungs.

1stPages_A.indd 38 7/22/20 10:41 AM

 has no vocal cords and is not a source The network of air and blood capillaries
of sound production. The trachea is that permeates the lung tissue gives it a
composed of cartilaginous or bony rings bright pink color and a spongy appear-
and, in most species, passes directly ance.
from the larynx to the syrinx. In some Branching off from the mesobron-
species, such as the Whooping Crane chus are several ventrobronchi, and
(Grus americana), the trachea is exten- from these extend the anterior air sacs
sively coiled, and its total length may be (interclavicular, cervical, and anterior
greater than that of the bird. The elon- thoracic), and two rows of several dorso-
gated trachea may function in sound bronchi. The ventro- and dorsobronchi
production by these birds, but it may in turn branch into many parabronchi,
also be important in humidifying the air which are small, parallel tubes several
during long-distance migrations. At the millimeters long and of uniform diam-
distal end of the trachea is the syrinx, eter. The walls of the parabronchi are
which is the organ of sound production permeated by hundreds of openings
in birds. into tiny branching and anastomosing
The syrinx is a complex structure, air capillaries, which are surrounded
reinforced by a cartilaginous skeleton, by a network of blood capillaries. The
with tympanic membranes on both its posterior end of a mesobronchus has
medial and lateral walls (fig. 2.15). Air branches to the posterior air sacs (poste-
movement past these membranes during rior thoracic and abdominal). All the air
expiration produces sound; the pitch of sacs are paired except the interclavicular.
the sound can be varied by contraction They are reconnected to the lung and the
of muscles running from the trachea to
the sternum and from the trachea to the
bronchi, which changes the tension on Fig. 2.15. Detailed structure of the syrinx of a
the membranes. Both the structure of the songbird.
syrinx and the musculature around it are
critical to the development of song. Poor
singers such as pelicans and vultures
have no syringeal muscles; ducks, geese,
gulls, and others have only one pair of
muscles, while songbirds have five to
nine pairs.
Two bronchi arise just posterior to
the syrinx. These relatively short tubes
are also reinforced with half rings of
cartilage and enter the lungs on their
ventral surface, passing through the
lungs as the mesobronchi (singular,
mesobronchus). The avian lung is
smaller than that of the mammal and
is a rigid structure whose volume does
not change during the respiratory cycle.

39

1stPages_A.indd 39 7/22/20 10:41 AM

 parabronchi by the recurrent ­bronchi. from the airstream. Proof that this sys-
The unidirectional pattern of air tem does produce greater efficiency of
flow through the avian lung depends on gas exchange is found in a comparison
all these structures. During inspiration, of ventilation rates and metabolic rates
air flows directly to the posterior air of some nonpasserines (relatively prim-
sacs through the bronchus and meso- itive land birds such as pigeons) and
bronchus. At the same time, air already mammals of comparable size. While the
present in the lungs is drawn through metabolic rates (oxygen consumption)
the parabronchi into the anterior air are about the same in nonpasserines
sacs. During expiration, the air from the and mammals, the ventilation rate
posterior air sacs is drawn into the lung (amount of air respired per minute) in
through the recurrent bronchi and the birds is 25% lower than in mammals.
air in the anterior air sacs passes out Only by extracting more oxygen from a
through the trachea. Because of this two- smaller quantity of air could birds match
step process, air flows continuously in the oxygen utilization of mammals.
one direction through the lung, during The improved pattern of air flow
both inspiration and expiration. through the lung and better extraction
Although there is no functional of oxygen give birds an advantage over
diaphragm separating the thoracic and mammals in oxygen-demanding situ-
abdominal cavities in birds, there is still ations, such as during intensive work
a pressure gradient generated by the or at high altitude. The statistics are
action of the respiratory muscles that impressively in favor of birds. Bird flight
drive air through the avian respiratory generally requires elevation of metabolic
system. When the inspiratory muscles rate well above that attained during
contract, the body volume and that of maximum exercise in mammals (9–12
the air sacs increase, creating a subat- times standard metabolism in birds and
mospheric pressure there, which draws 6–10 times in mammals); moreover,
air into them. Conversely, when the certain types of flight, such as hovering,
expiratory muscles contract, the volume demand even higher expenditures, up to
of air in the air sacs is compressed, gen- 20 times standard metabolism. Migrat-
erating a pressure slightly higher than ing birds typically fly below 1500 m, but
atmospheric, which drives the gases several species cross high mountain
either into the lung or out the trachea passes during their migration. Bar-
and mouth. headed Geese (Anser indicus) have been
Another unique difference in the observed flying from sea level to altitudes
avian respiratory system is the cross-cur- of 8000 m in just a short period.7 House
rent flow of blood and air in the capillar- Sparrows (Passer domesticus) and lab
ies, which promotes greater efficiency of mice were exposed to a simulated alti-
oxygen extraction and greater removal of tude of 6100 m in a hypobaric chamber.8
carbon dioxide than in the mammalian Whereas the mice were comatose in this
chapter 2

system. Air flows through the parabron- rarefied atmosphere, the House Spar-
chus at right angles to the flow of blood, rows could not only fly but could gain
so that carbon dioxide is continually altitude. Neither species was acclima-
added and oxygen continually removed tized to the high altitude before the trial.

40

1stPages_A.indd 40 7/22/20 10:41 AM

 Circulation neck, and head. Running posteriorly, the
aorta gives rise to arteries that supply the
Moving the fuel from the digestive tract viscera, the posterior appendages, and
and the oxygen from the lungs to meet the back and tail musculature, simi-
the energy and oxygen requirements lar to those in mammals. The venous
for flapping flight requires an efficient return to the heart is also similar to that
circulatory system. The heart and the in mammals, except that birds possess
arrangement of the major vessels in a renal portal system. Venous blood
birds are much the same as in mam- returning from the limbs via the iliac
mals, with a few notable differences. veins can enter the kidneys via the renal
The avian heart is a four-chambered, portal veins, which break up into capil-
double-barreled pump that keeps pulmo- laries that surround the renal tubules (in
nary and systemic blood separated, as mammals, this capillary bed is arterial,
in mammals. Thin-walled atria receive fed by the efferent arteriole). The renal
venous blood from the body (right portal circulation is not obligatory; flow
chamber) and the lungs (left chamber) is apparently controlled by a renal portal
and pass it to thick-walled ventricles. valve. The renal portal valve is the only
The right atrium is much larger than the intravascular structure in vertebrates
left in birds, but the wall of the left ven- that contains smooth muscle and has
tricle is two to three times thicker than an autonomic nerve supply. When the
that of the right, which reflects the pres- valve is open, blood passes through the
sures generated by the ventricles. The iliac vein and renal portal vein to the
blood pressure generated by the heart posterior vena cava and the heart. When
and sustained by the arterial vessels is the valve is closed, blood passes through
somewhat higher in birds than in mam- either the cranial renal portal vein into
mals: in turkeys about 200/​150, and in the kidney or the caudal renal portal vein
chickens about 175/​150. Blood pressure that passes to the hepatic portal system
varies as heart rate does in response to via a coccygeomesenteric vein. In vivo
exercise, fright, temperature, age, and radiographic studies have shown that
size (see discussion below). These high the renal portal valve is open about 74%
pressures can occasionally be disastrous of the time and closed about 26% of the
General Traits of an Avian Flying Machine
to birds; intensely excited birds have time.
died of ruptured aortas or ventricular The blood of birds is approximately
walls. Thus, birds seem to operate very 80% water and is composed of the
close to the mechanical limits of their same cellular elements and dissolved
circulatory system. salts and proteins as mammalian blood.
The circulatory pathways in the bird The erythrocytes (red blood cells) and
resemble those in the mammal, with thrombocytes (equivalent to mammalian
one major exception. The aorta arises platelets) are nucleated cells in birds and
from the left ventricle but turns to the tend to be somewhat larger than their
right in birds, instead of to the left as it mammalian counterparts. Numbers and
does in mammals. Two large brachio- size of erythrocytes vary among birds. In
cephalic arteries branch from the aorta general, active fliers and smaller-bodied
and carry blood to the wings, thorax, species tend to have more and smaller

41

1stPages_A.indd 41 7/22/20 10:41 AM

 erythrocytes. The granular and agranular changes are impressive, but far less
leukocytes are similar in birds and mam- dramatic than the 6- to 10-fold increase
mals, but their relative numbers are in heart rate observed in a thoroughbred
higher in birds. Blood proteins are vari- horse at full gallop. Heart rates can vary
able in birds, depending on sex, age, and tremendously from moment to moment
reproductive status. For example, plasma in birds, usually because of excitement,
proteins are generally lower in males and for this reason are not good indi-
than in females and are greatly elevated cators of the bird’s level of activity. For
in laying females because of increases in example, the sight of a hawk can cause
lipids, iron, and calcium-binding pro- the heart rate of turkeys to rise from 175
teins. beats per minute to over 300 within one
Certain adjustments of the avian car- minute.
diovascular and respiratory systems per- Many birds have extremely large
mit birds to engage in such strenuous hearts in proportion to their body size.
activity as flight. Oxygen is made avail- In fact, avian heart weight as a percent-
able to exercising muscles by increasing age of body weight is much greater than
respiratory exchange: generally, birds that of mammals of similar body size.
increase their resting oxygen consump- The heart of a House Sparrow (Passer
tion by 9 to 12 times during flight. This domesticus) represents 1.34% of its body
is accomplished by increasing the rate weight, while the heart of a lab mouse
and depth of breathing. It is possible (approximately the same body weight)
that the contraction of the flight muscles makes up 0.5% of its body weight.
is an additional aid to internal air move- Generally, heart size of smaller birds is
ment during flight, especially in the air larger in proportion to body size than
sacs and parabronchi. Cardiovascular that of larger birds. The large heart may
adjustments to increase oxygen delivery be adaptive for two reasons: a large
involve increases in heart rate, stroke heart needs to contract less to eject a
volume (the amount of blood pumped at given volume than a smaller heart; and
each beat), and the difference between a large heart represents a reserve of
arterial and venous oxygen concentra- volume that can be pumped on demand,
tion in the blood (the latter achieved by that is, by increasing stroke volume.
decreasing venous oxygen tension). The latter provides a basis for quickly
Heart rate of birds is determined by increasing oxygen delivery, even without
body size and activity level. Generally, concomitant changes in respiration. In
heart rates of small birds (and younger general, heart size in all vertebrates is
birds) are proportionately faster than determined primarily by the amount of
those of larger birds (or older birds), work the heart is asked to do. Heart size
and the increase in heart rate during is larger in birds living at high altitude,
flight is less in small birds (about two where the decreased oxygen pressure in
times resting) than in large birds (three the atmosphere necessitates faster cir-
chapter 2

to four times resting). The resting heart culation. It is also proportionately larger
rate of Herring Gulls (Larus argentatus) in birds that spend a great proportion
increased from 130 beats per minute of time flying, and in temperate-zone
to over 600 when the birds flew. These residents during the winter.

42

1stPages_A.indd 42 7/22/20 10:41 AM

 The combination of a relatively large important role of the kidney is mainte-
heart and fast heart rate means that nance of water and salt balance, which is
birds can pump a large quantity of blood discussed in connection with extremely
per unit time (cardiac output). Birds hot and dry environments later in the
have a greater cardiac output per body book.
mass than mammals and can reach The urinary organs of birds con-
much higher levels during exercise than sist of paired kidneys and ureters that
mammals can. For example, a flying transport urine to the cloaca. Several
Budgerigar (Melopsittacus undulatus) had unique features of the avian kidney set
a cardiac output more than seven times it apart from the mammalian type. The
the maximum attained by humans or trilobed kidneys are located posterior to
dogs. the lungs and recessed in bony depres-
Further increases in oxygen delivery sions of the synsacrum. Each lobe is
in birds can be achieved by unload- made up of lobules, composed of a large
ing more of the arterial oxygen at the cortical mass and a smaller medullary
tissues, resulting in lower venous mass within, and is drained by a single
oxygen tension. The difference between urethral branch. Within each lobule is a
arterial and venous oxygen tension central vein around which the nephrons
increases about two times during flight are arranged in a radial pattern. Neph-
in birds. Thus, the maximum potential rons are composed of glomeruli (sin-
for increase in oxygen delivery above gular, glomerulus), where renal arterial
the resting level is about 12 times in blood is filtered to produce a protein-free
birds (a 4-fold increase in heart rate × filtrate, and tubules that reabsorb nutri-
a 1.5-fold increase in stroke volume × ents and much of the water, leaving the
a 2-fold increase in the arterial-venous waste products in a concentrated form.
oxygen difference). This potential nicely The tubules are surrounded by a venous
matches the 9- to 12-fold increase in capillary bed that derives from the renal
oxygen consumption measured for birds portal vein (rather than from an arterial
during flight. source as in mammals). The cortex of
each lobule contains both nephrons
Excretion without loops of Henle, similar to those
General Traits of an Avian Flying Machine
of reptiles, and other nephrons, deeper
In the process of converting foodstuffs in the cortex, that have loops of Henle
to metabolic fuel, certain waste prod- and are of the mammalian type. The
ucts accumulate that must be excreted. loops of Henle extend into the medullary
We have already discussed elimination area of the lobule and are exposed to
of carbon dioxide by the lungs and of an osmotic gradient formed by a renal
unmetabolized food by the digestive countercurrent multiplier system similar
tract via the cloaca. However, nitroge- to that found in mammals. Collecting
nous waste products that result from ducts drain both types of nephrons and
intermediary metabolism in other pass through the medullary area into
organs, such as the liver, must be elim- a branch of the ureter. Urinary waste
inated by the urinary system. Another passes down the ureter aided by per-

43

1stPages_A.indd 43 7/22/20 10:41 AM

 istaltic contractions and empties into Muscles
the cloaca at the urodeum. From there
the waste may be passed back up the The organ systems we have described
colon and ceca, and so the final excretory above generate fuel for energy and
product is modified by the actions of the remove the waste produced, but they
digestive tract. The uric acid salts tend cannot directly make a bird move.
to precipitate and form a white coating For that we need muscles acting on a
or cap around the fecal material. This is skeletal system and on the feathers. The
what gives bird excreta their characteris- average bird has nearly 200 muscles,
tic two-colored appearance. most of which are paired; that is, they
The primary nitrogenous waste occur on both sides of the body. Most of
product in birds is uric acid, which these muscles, such as those attached
constitutes 52%–88% of the total nitro- to feathers, are very small compared to
gen of the urine of ducks and chickens. those used in flying or walking. Even the
Uric acid is synthesized in the kidney ratio of flight muscles to walking mus-
and liver, from which it is transported to cles varies with the lifestyle of the bird;
the kidney via the renal arterial or renal strong fliers may have 21% of their body
portal system. It is both filtered by the mass in flight muscles, while in nonfli-
glomerulus and secreted by the tubules ers less than 10% of the body mass may
into the filtrate, so that it becomes highly be flight muscle.
concentrated in the urine. Because uric Birds are distinctive in having the
acid, unlike urea, is not toxic at high bulk of their musculature placed ven-
concentrations, less water is needed to trally and near their center of gravity,
keep it in solution than is needed by an adaptation for flight (fig. 2.16). The
mammals to maintain urea in solution fused vertebrae take the place of the
at nontoxic levels. However, the uric dorsal musculature and provide resis-
acid salts must be fairly liquid in order tance to the contraction of the powerful,
to pass down the ureter. If the bird ventrally placed flight muscles. The bulk
becomes dangerously dehydrated, the of the limb musculature is placed at the
uric acid paste that forms in the ureter proximal end of the limb, which keeps
may eventually block it. Excess water the appendage light and the weight
in urinary waste can be reclaimed in closer to the bird’s center of gravity.
the cloaca, the colon, and the ceca (as Two individual muscles make up
described above). the bulk of the mass of flight muscles:
The advantage of uric acid excretion the large pectoralis muscle, which
is that ultimately more nitrogen can be pulls the wing downward and provides
excreted per milliliter of water lost. A the propulsive force, and the smaller
mammal that eats 1 g of protein forms supracoracoideus, which pulls the wing
320 mg of urea and uses 20 ml of water up (fig. 2.17). The supracoracoideus is
to excrete that nitrogen in an isotonic located beneath the broader and more
chapter 2

solution. A bird can excrete the same superficial pectoralis. Both muscles orig-
amount of nitrogen (in uric acid) using inate on the keel of the sternum. The
only 1 ml of water in an isotonic solu- fact that neighboring muscles can pull
tion. the wing both up and down is explained

44

1stPages_A.indd 44 7/22/20 10:41 AM

 General Traits of an Avian Flying Machine

Fig. 2.16. Major muscles of a chicken, showing contrast, inserts on the lower surface of
how heavy muscles are concentrated near the the humerus. The supracoracoideus is
center of gravity to aid in flight. best developed in birds that utilize steep
takeoffs, in those that engage in hover-
ing where the back or recovery stroke
by a tendonous attachment of the also provides lift, and in soaring birds,
supracoracoideus that passes through a where it is used for rapid adjustments of
foramen in the pectoral girdle over the the wing position against varying wind
scapula and coracoid to insert on the forces in order to keep the wing profile
top of the humerus. The pectoralis, in horizontal.

45

1stPages_A.indd 45 7/22/20 10:42 AM

 Fig. 2.17. View of the two major flight muscles The most complex set of muscles
(pectoralis on the outside, supracoracoideus is that devoted to controlling the varied
beneath it) and their attachment to the movements of the head and neck. These
humerus to control flight. Note that the muscles are rather short and are often
pectoralis is attached to the bottom of the subdivided and attached to one another
humerus to provide power on the downstroke, by means of fascia. Contractions of one
while the supracoracoideus loops around the
muscle are tempered by many others
bones and attaches to the top of the humerus,
and produce quite variable results. Like-
such that contraction of the supracoracoideus
wise, the tail musculature may be com-
pulls the wing upward.
plex, especially in birds such as lyrebirds
or some gallinaceous species whose
The leg muscles are also concen- sexual display depends on manipulation
trated proximally, with the bulk being of the tail feathers. The pygostyle, to
located in the thigh, and fewer found which tail feathers attach, is moved by
lower along the tibiotarsus. The muscles several pairs of muscles, and there are
in the thigh and lower leg can flex and muscles attached directly to the follicles
extend the tarsometatarsus and digits by of the tail feathers themselves.
means of long tendons that run inside Smooth muscles in the dermis
and outside of the lower joints. For of the bird attach to the feather folli-
example, plantar tendons extend from cles and are responsible for feather
flexor muscles in the thigh down the erection and depression. Generally, a
back of the tarsometatarsus and insert given muscle may be attached to more
on the digits. Contraction of the mus- than one follicle, and any one follicle
cles causes closure of the foot (flexion), may have two to several dozen pairs of
chapter 2

the basis for the perching reflex. This antagonistic muscles attached to it. The
arrangement of muscle and tendon movement of feathers is critical during
allows birds to rest and sleep while flight but is also important for tempera-
tightly gripping their perch. ture regulation (regulating insulation

46

1stPages_A.indd 46 7/22/20 10:42 AM

 and heat loss), brooding, defecation, and to note that none of them can function
sexual display. alone. Coordinating all the activities
As most anyone who has celebrated of the organ systems is the job of the
Thanksgiving knows, bird muscle is nervous system and endocrine glands.
dark (red) or white. This is due to the Their control functions range from the
predominance of red or white muscle simple coordination of the movement of
fibers within a muscle, although many a single feather to the complex coordina-
muscles are mixtures of both types. tion of all the muscles in flight. To these
White fibers are found in muscles that must be added controls of the short-term
are used for short, powerful bursts of navigational ability that allows a bird
action. They are large-diameter fibers to avoid a tree branch or to land prop-
with few capillaries and little myoglobin erly. At a higher level are the long-term
(which binds oxygen). They use gly- controls that tell migratory species when
cogen stores to produce rapid, strong and where to travel and how to get there.
contractions but fatigue easily because Inputs from the senses of taste, touch,
they do not have the aerobic capacity to sight, smell, hearing, and perhaps mag-
sustain the contraction. White fibers in netism must be synthesized, along with
the breast muscle of some gallinaceous appropriate controls of metabolism and
birds, such as grouse, enable the bird to other bodily functions. Obviously, the
make rapid, steep takeoffs, but the mus- control system is exceedingly complex,
cles become exhausted after several take- and it is not yet completely understood
offs in succession. In contrast, red fibers in birds or mammals.
are found in muscles that can sustain Most people do not delight in being
contractions for long periods. They are called “bird brained” because of the
thinner in diameter than white fibers, connotation of stupidity. However, the
have many mitochondria and blood rather pronounced differences between
capillaries, are high in myoglobin and avian and mammalian brain structure
fat content, and use enzymes associated are not related to differences in their
with aerobic metabolism to sustain a intelligence. Rather, different parts of an
contraction. Pectoral muscles of long-dis- avian or mammalian brain may perform
tance migrants are usually composed similar functions. A team of neurosci-
General Traits of an Avian Flying Machine
entirely of red fibers. Although white entists recently revisited the whole issue
muscle dominates in the chicken and its of which group of animals is smartest.10
relatives, there are some strange excep- Given new insights into what birds can
tions to the general pattern of muscle do and a rethinking of the extent that
color, such as the appearance of white brain structure is correlated with brain
muscle in the Blue-headed Quail Dove function, these neuroscientists put birds
(Starnoenas cyanocephala), whose pigeon higher up in the intellectual pecking
and dove relatives all have red muscle.9 order. For example, songbirds can learn
up to 2,000 different melodies. Florida
Control of the Avian Machine Scrub Jays (Aphelocoma coerulescens)
can remember things that happen at a
We have looked at most of the organ specific time and place, something once
systems individually, but it is important thought unique to humans. Experiments

47

1stPages_A.indd 47 7/22/20 10:42 AM

 show that pigeons and crows can iden- stimuli and pass it on to the CNS; or
tify individual people and distinguish efferent (motor) fibers, which pass infor-
between those they find dangerous mation from the CNS to organs or mus-
and those that they feel are safe to be cles. Peripheral nerves traveling to and
around.11 African Gray Parrots (Psittacus from the muscles are called somatic;
erithacus) can use words and numbers those traveling to and from the viscera
correctly in conversation with humans. and skin (glands) are called autonomic.
Pigeons can memorize up to 725 dif- The most obvious difference
ferent visual patterns, choose between between bird and mammal brains lies
human-made and “natural” objects, and, in the cerebral hemispheres (fig. 2.18).
most astonishingly, distinguish between In mammals, the hemispheres consist
Picasso and Monet, and cubism and almost entirely of neocortex, convoluted
impressionism.12 New Caledonian Crows folds of gray matter that cover a thick
(Corvus moneduloides) in the wild rou- layer of white matter tracts and encircle
tinely make and use two different types the more primitive vertebrate structures
of tools to get food. A crow reared in an of basal ganglia, thalamus, midbrain,
Oxford University laboratory stunned and brainstem. The neocortex in mam-
scientists with its knowledge of phys- mals is important in the development of
ics when it took a length of wire, bent learned behaviors and could therefore be
it into a hook, and started fishing out termed the foundation for intelligence.
tidbits from a tube.13 Pigeons have been In birds, the neocortex has always
suggested to rival primates in numerical been considered undeveloped. The
competence.14 Birds can do many amaz- hemispheres consist of a thin and
ing things that it would be difficult to get rather flat layer of gray matter covering
other mammals such as rats or dogs to a greatly elaborated structure called the
do, so we must change our old concept corpus striatum that derives from the
of “bird brained.” A recent paper sug- basal ganglia (fig. 2.18). Different layers
gested that perhaps we should consider of the corpus striatum are associated
birds to be “feathered apes.”15 with visual integration, pattern discrim-
ination, visually controlled defensive
The nervous system reflexes, eating, vocalization, and hear-
ing, as well as complex instincts related
The nervous system can be split ana- to reproduction, such as copulation, nest
tomically into two divisions, the central construction, incubation, and feeding of
nervous system (CNS), consisting of the the young. In the past, this dominance
centrally located sense organs, the brain, by the corpus striatum involved instinc-
and the spinal cord; and the peripheral tive behaviors, responses that are largely
nervous system (PNS), consisting of the stereotypical and mechanical; the area
cranial and spinal nerves serving the of the avian brain that dealt with cog-
glands, muscles, heart and other visceral nitive behavior was considered small.
chapter 2

organs, and the sense organs. Periph- Recent evaluations of the function of the
eral nerves may carry afferent (sensory) avian brain suggest that it has a large
fibers, which receive information from area (perhaps 75% of the brain) where
organs in the body or from external cognitive behavior can originate, per-

48

1stPages_A.indd 48 7/22/20 10:42 AM

 haps as large an area as is found in most
­mammals.16
Within the cerebral hemispheres lie
the thalamus and midbrain. The thala-
mus, as in reptiles and mammals, is a
primary visceral reflex center. It controls
some visceral reflexes via connections
with neurons in the medulla and mod-
erates certain neuroendocrine reflexes,
such as hunger and thirst, through its
connection with the ventrally located
pituitary gland. The thalamus also acts
as a relay center for sensory informa-
tion passing from the spinal cord to the
corpus striatum.
The other major parts of the avian
brain are the olfactory bulbs, optic lobes,
cerebellum, and medulla. The olfactory
bulbs and optic lobes are sensory and
Fig. 2.18. Changes in our understanding of the
integrative in function, coordinating
composition and function of the bird brain
the olfactory and visual senses, respec-
when compared to a human brain (top). The
tively. The large optic lobes reflect the classic view of a bird brain (bottom left) was
importance of the visual sense to birds. that it was dominated by the ability to do
A dense layer of gray matter in the optic instinctive behaviors (called pallial behaviors
tectum receives information from the and shown in shades of green) but was limited
eyes, head, and body. The importance in its ability to do complex, cognitive behaviors
of this midbrain area is illustrated by (called striatal and shown in red). Recent work
decerebrate pigeons (that is, those has shown that the cerebrum of a bird has a
without the cerebral hemispheres) that massive region that supports striatal behavior
can still fly and land properly. Recent (PBS 2005).
work has added a new component to
General Traits of an Avian Flying Machine
brain function with the discovery of a
light-sensitive portion at the top of the dant sensory input from the inner ear
brain; this “third eye” appears to be the and the body, maintains body equilib-
mechanism with which the bird tracks rium, and coordinates both stereotyped
photoperiod through the year.17 Also, a and nonstereotyped muscle movements.
region of the brain that serves as a mag- The medulla, located at the top of
netometer has recently been discovered, the spinal cord, controls simple vis-
allowing a pigeon to encode information ceral reflexes, such as those involved in
from the earth’s magnetic field for use in breathing and the maintenance of heart
orientation and navigation.18 rate and blood pressure. Large tracts
The cerebellum is large and well of white matter in the medulla link the
developed in birds, as might be expected neurons of the spinal cord with those in
of these aerial acrobats. It receives abun- the cerebellum, midbrain, and cerebral

49

1stPages_A.indd 49 7/22/20 10:42 AM

 hemispheres. Eight of the cranial nerves vores such as flycatchers and nightjars
enter at the medulla. often have pronounced rictal bristles
The avian spinal cord, unlike that of that help in capturing flying insects.
mammals, extends the length of the ver- The bills of many birds are also highly
tebral column and is somewhat simpler sensitive, with touch receptors com-
in structure than in other vertebrates. posed of Herbst and Grandry corpuscles.
The sensory tracts are notably smaller The latter is particularly true of birds
than the motor tracts in the cord, per- such as kiwi, snipe, and sandpipers that
haps because there are fewer sensory probe into mud or sand and catch prey
endings in the skin. The cord is enlarged by feeling it with touch receptors located
in the cervical and lumbosacral regions at the tip of the bill. Ducks can separate
because of the many neurons that give sand from food items by using the touch
rise to axons going to the limbs. In these receptors in their bill. Wood Storks
areas of the cord are reflex centers that (Mycteria americana) can close their beak
perform some of the integration of infor- on a live fish only 0.019 second after
mation involving wing and leg move- contact. By comparison, the blink reflex
ments. The thrashing movements of a in humans takes 0.04 second. Wood-
beheaded chicken attest to the impor- peckers have a very long, barbed tongue
tance of cord reflexes as controllers of that can find grubs in bark through the
major movements in birds. However, sense of touch. It was long thought that
these lower control centers can be over- these grubs were speared by the barbs,
ridden by motor impulses from higher but recent work suggests that the wood-
centers in the brain. pecker uses sticky saliva to catch the
grubs and pull them out.
The sense organs Although we will discuss avian
reproduction later in the book, there are
The relative importance of the senses two important aspects of the sense of
varies greatly among groups of birds, touch that are associated with reproduc-
depending on a suite of characteristics tion and should be noted here. The first
related to the food habits, behavior, is the brood patch, a bare area on the
migration, and other traits of the spe- belly of birds that allows direct contact
cies. A wonderful review of these traits between the incubating bird and the
appears in the book Bird Sense by Tim developing embryo. Making tactile con-
Birkhead (2012); many of the examples tact is an important part of incubation,
below are from this book. and many species determine their clutch
Touch. Although the sense of touch has size by the sensory contact between the
not been considered highly developed eggs that have been laid and the brood
in general, we have probably underesti- patch. These birds, termed indetermi-
mated the importance of touch to many nate layers, will continue to lay eggs
birds. Skin sense organs associated until the birds perceive that they have
chapter 2

with flight feather follicles are critical laid enough eggs through this contact.
to coordinating flight, and filoplumes Finally, the sense of touch is important
scattered throughout the plumage are to sex in birds, as all avian sex involves
also of a sensory nature. Aerial insecti- some sort of tactile stimulation between

50

1stPages_A.indd 50 7/22/20 10:42 AM

 the cloaca or penis of a male and the be led to a food source by the release
cloaca of a female. of ethyl mercaptan fumes in their
Taste. The sense of taste is poorly flight path. However, once in the gen-
developed in birds. Taste receptors do eral area of a food source, the vultures
not occur in visible aggregates like the rely on their eyesight to find the exact
taste buds of mammals, but taste buds location. Leach’s Petrels (Oceanodroma
are found on the sides of the tongue, leucorrhoa) apparently home to their
in the bill and soft palate, and next to island nesting locations at night by
the salivary glands. Pigeons have only flying upwind. Their homing ability
50–60 taste buds, chickens about 300, was diminished when olfactory nerves
Mallards about 400, and African Gray were severed or their nostrils plugged.
Parrots 300 to 400, compared to 10,000 African honeyguides (Indicatoridae)
in humans. But this limited number of are also distinctive in using olfaction
taste buds may suffice for the choices to home in on warm beeswax and can
made by different birds. Nectar-eating be attracted to the fumes of a lighted
species can discriminate types and beeswax candle from great distances. It
amounts of sugar in flowers, and fruit has been suggested that a kiwi (Apteryx)
eaters can tell ripe fruit from green can smell a worm through 15 cm of soil.
fruit. Insect-eating birds can tell the Some recent work suggests that the oil
difference between tasty caterpillars and of the preen gland varies in the amount
insects and those that express chemical of male-like body odors; males with a
defense systems through the foods they higher abundance of these mating com-
eat. Some birds are also insensitive to pounds attracted higher-quality females
spicy and bitter tastes and will consume and had a greater number of successful
quinine, formic acid, capsicum peppers, young than males who did not smell
and other distasteful and irritating sub- quite so good.19
stances. However, many birds are able to Vision. Although taste, touch, and smell
discriminate salt and will preferentially may be generally underdeveloped in
choose it when they have been raised birds, the senses of hearing and vision
on a salt-free diet, or avoid it when it is are highly developed. In fact, vision
given in high concentrations in drinking reaches its zenith in birds, where the
General Traits of an Avian Flying Machine
water. For example, most birds without eyes are very large, and the optic lobe
a nasal salt gland will refuse to drink is the largest part of the midbrain. The
water more salty than plasma (about large size of the eye (15% of the head
0.9% salt). Even birds with nasal salt weight of a starling compared to 1%
glands prefer pure water to saline. in humans) accommodates increased
Smell. The sense of smell in birds was numbers of photoreceptors and permits
once thought to be poorly developed, increased visual acuity.
especially in the more advanced song- The general construction of the
birds. However, researchers have found avian eye follows the vertebrate plan but
that it is a highly developed sense in has many adaptations to improve visual
some vultures, the kiwi, albatrosses, acuity. The wall is constructed of three
petrels, and a few other species. Migrat- layers: an inner sensory layer, the retina;
ing Turkey Vultures (Cathartes aura) can a middle, vascular layer that includes

51

1stPages_A.indd 51 7/22/20 10:42 AM

 the choroid, iris, and ciliary body; and possesses much better point-to-point
an external protective layer, the sclera resolution of an image than the mam-
and transparent cornea (fig. 2.19). A malian eye. Rods are concerned with
unique organ of the avian eye is the dim-light vision, and the eyes of noctur-
pecten, also found in a simpler form in nal birds generally have more rods than
reptiles. It consists entirely of capillaries cones. The cones function in both color
and pigmented cells that project variable discrimination and visual acuity, and
distances in different species into the vit- in birds, as in other vertebrates except
reous body in the posterior chamber of placental mammals, contain oil droplets.
the eye. The varied functions ascribed to The droplets are pigments dissolved in
the pecten include serving as a nutritive lipid and are usually yellow or red. They
organ for the avascular retina, regulating may serve as ultraviolet screens or as
intraocular pressure, absorbing reflected color filters that modify the cone absorp-
light, aiding detection of movement tion spectrum, thereby improving color
because of the shadow it casts on the discrimination. However, oil droplet
retina, providing an intraocular shade pigments may not be essential for color
against sun glare, and acting as a mag- vision; Japanese Quail (Coturnix japon-
netic sensor for navigation. Birds also ica) unable to synthesize the carotenoids
have a third eyelid called the nictitating in these droplets still have normal color
membrane. This highly elastic mem- discrimination.
brane is generally opaque, serves as a The inner layers of the retina consist
protective layer, and bathes the eye with of the bipolar and ganglion cells that
fluids when the eyes are open. The outer make synaptic connections with the rods
eyelids are closed only during sleep. and cones. Birds have more of these
However, in some diving birds the nicti- cells than do mammals, and the cones
tating membrane has a clear spot in the are generally connected in a one-to-one
center. It is drawn across the eye during fashion with their bipolar cell and gan-
a dive and acts as a contact lens over the glion cell, which assures a point-to-point
cornea that permits vision underwater. representation of the original image in
The sensory layer of the bird eye the brain. The sharpest vision occurs in
is chiefly responsible for the greatly the cone-rich area known as the fovea,
enhanced visual acuity of birds. It is as is the case in mammals. About half
organized just as the mammalian retina of bird species have two foveae in the
is, with the rod and cone photorecep- eye; one may be located centrally in
tors in the outermost layer of the retina the back of the eye to the side of the
oriented away from incoming light optic nerve, and another temporal to
and with the tips in proximity to the and above the optic nerve. While the
light-absorbing choroid layer. However, former may be used when the bird is
there are many more rods and cones standing and looking straight ahead,
per millimeter of avian retina than in it uses the latter when flying, permit-
chapter 2

even the most keen-eyed mammal. The ting the bird to see beneath it without
tighter packing of the photoreceptors moving its head. Some birds have a
and the lack of vascular interruptions horizontal streak across the center of the
in that surface mean that the avian eye retina with a fovea at each end. This is

52

1stPages_A.indd 52 7/22/20 10:42 AM

 Fig. 2.19. The standard structure of a
bird eye and variation in eye shape, eye
placement, and field of view in birds.
Owls have very tubular eyes set close
together in the front of the head. This
provides a large area of binocular vision
(blue), but a relatively narrow field of
view (blue area plus the white areas of
monocular vision) and a broad blind
area (black). Hawk eyes are somewhat
less tubular and are placed on the sides
of the head; they have somewhat less
binocular vision (blue) but a much
broader field of view and a smaller
blind spot. Most species of birds have
relatively oval eyes placed on the sides
of the head. This provides vision that
approaches (waxwing or swan) or
exceeds (woodcock) 360° in coverage,
with little binocular vision but also
a small blind spot, except in the
woodcock, where placement of the eyes
high on the head provides a full field of
view but small areas of binocular vision
both in front and in back of the bird.

1stPages_A.indd 53 7/22/20 10:43 AM

 found in birds that fly in open country Since the woodcock eats worms that it
and allows them to scan the horizon finds by probing the soil with its long,
without moving the head or eyes. The flexible bill, depth perception is probably
margins of the fovea are thickened and not a major problem. Such is also true
contain great numbers of bipolar and for pigeons, as the fruits and seeds they
ganglion cells, whereas the fovea itself eat do not run away. In some species
is a depression in the retina composed that use their eyes primarily for predator
of a linear arrangement of thinner and detection, the vision to the rear equals
longer cones. Some researchers believe that to the front.
that the walls of the fovea act as a convex In species that require good visual
lens that magnifies the retinal image, acuity to capture prey, overlapping fields
whereas the extremely thin cones within of view and good depth perception are
the fovea produce resolving power at important. Not surprisingly, birds of prey
least eight times greater than a human’s. have eyes in the front of their head, fac-
The shape, placement, and flexibility ing forward. Binocular vision reduces the
of the eye vary greatly among birds (fig. total field of vision but greatly increases
2.19). Owls and many other nocturnal the depth perception of these birds,
birds have large, tubular eyes with a where the difference between success
greater surface area of rods to aid night and failure in prey capture requires exact-
vision. Diurnal species with excellent ing standards. By comparison, the overall
long-distance resolution, such as crows, field of view is fairly wide in the Euro-
have a globose eye. The more typical eye pean Kestrel (Falco tinnunculus; 250° with
shape is flattened, as in most small diur- 50° of overlap), but in owls the emphasis
nal birds. In many of these latter species, on binocular vision results in an overall
the eyes are very important in detecting visual field of only 60°–70° with 50° of
predators, and the eyes are shaped so overlap between the eyes. Owl eyes are
that they possess a large field of view. In also fixed in the socket, so the birds must
addition, the eyes are placed on the head rotate their head to scan the landscape,
so that there is little overlap between the an ability aided by an extremely flexible
area seen by each eye. The most extreme neck. Species such as herons and bit-
eye placement may be that of the wood- terns that use their bill to capture prey
cock (Scolopax), whose eyes are on the below them have widely spaced, down-
sides and near the top of the head. This ward-turned eyes on the sides of their
allows 360° vision, with only tiny areas head. This allows some binocular vision
where binocular vision occurs. The eyes in bitterns, but only when the bill is
of a pigeon are not quite as high on the pointed upward.
sides of the head and provide a total field Birds are capable of adjusting their
of view of 340°, with just a small blind visual acuity over a wide range of dis-
spot behind the head. This wide field tances. This is called visual accommoda-
of view comes at the expense of depth tion and is accomplished by modifying
chapter 2

perception, which depends on overlap- the shape of the soft lens and cornea.
ping fields of view from the two eyes. Most birds have a visual range of 20
It has been suggested that birds with diopters (near to far), which is twice that
these eyes may see two separate images. of humans. Some aquatic species like

54

1stPages_A.indd 54 7/22/20 10:43 AM

 the American Dipper (Cinclus mexi-
canus) have a range of 50 diopters.
Hearing and equilibrium. The avian
sense of hearing is also highly developed
and reaches its epitome in certain owls
that can catch prey in total darkness
and in several species that can echolo-
cate. The ear is the sensory organ for
both hearing and equilibrium and has
anatomical features in common with
both reptiles and mammals (fig. 2.20).
Sound waves enter the external ear,
which may or may not have a protective
covering, and pass down the canal to the
eardrum. Vibrations from the eardrum
are passed through the middle ear by
the one middle ear bone (mammals
have three ear bones), the columella, to a
membranous oval window on the inner
ear. Here, vibrations are passed to the
fluid chambers of the complex inner ear
Fig. 2.20. Location (top) and structure
organ called the membranous labyrinth.
(bottom) of the inner ear of a typical bird.
This structure in birds is very similar to
that in crocodiles, among their closest
reptilian relatives. of mammals cannot. These hair cells
Sensory areas in the three semi- enable birds to discriminate the tem-
circular canals and the utriculus and poral properties of sounds exceedingly
sacculus are important in the perception well. In fact, their temporal resolution
of movement and position, especially of sounds is about 10 times better than
of the head. Information from the hair that of humans. For example, it has been
cells in these areas is integrated with determined that single auditory neu-
General Traits of an Avian Flying Machine
that from the eyes and proprioceptors in rons of birds can discriminate discrete
the body to aid in maintenance of body sounds separated by as little as 0.6
posture and balance. millisecond, which would seem to be
At the base of the membranous one tone to the human ear.20 The range
labyrinth is the cochlea, a slightly curved of frequencies that birds hear is variable
bony tube, in which the organ of Corti and for the most part is very similar
and the auditory receptors are located. to that of most mammals (excluding
Although the cochlea of the average bird bats). Sounds in the range of 1,000 to
is only 1/10 the length of that of a typical 4,000 Hz are heard best, but sensitivity
mammal (which has a coiled cochlea), extends to about 30,000 Hz. Birds can
birds have about 10 times as many also hear extremely low frequencies of
hair cells per unit of length. Avian hair sound; homing pigeons, for example,
cells also can be replaced, while those can hear frequencies as low as 0.05 Hz,

55

1stPages_A.indd 55 7/22/20 10:43 AM

 including those associated with thunder- almost silently toward it. The sounds of
storms, earthquakes, and ocean waves. the wings in flight are muffled by the
Some researchers propose that these fringed leading edge of the primaries,
sounds may be important sources of and generally they are lower in frequency
navigational or meteorological informa- (less than 1,000 Hz) than the sounds
tion during migration. made by the prey.
It is their highly refined sense of Echolocation is another modifica-
hearing that has made owls so success- tion of hearing in birds that is found to
ful in their nocturnal niche. In species various degrees in some cave-dwelling
such as the Barn Owl (Tyto alba), the swifts, as well as in some nocturnal
ability to define the presence and move- hunters such as Oilbirds (Steatornis
ments of prey has been so refined that caripensis) and Galapagos Swallow-tailed
an owl can catch prey in total darkness.21 Gulls (Creagrus furcatus). These birds
Barn Owls have an external ruff of emit short clicks between 4 and 7 Hz,
feathers that focuses sounds the way which they use as bats do for navigation
a satellite dish does and directs them in the dark.
into the external ear canal (fig. 2.21). Recent studies have possibly discov-
Fleshy lobes bordering the ear may also ered a set of magnetic sensory organs
help direct the sound into the ear canal, that include a part of the inner ear of the
much as a cupped hand behind the ear pigeon,23 plus receptors in the eye and
would. The ear openings are asymmet- the upper beak that may allow the bird
rical in location, one above the midpoint to make a map. A chain of magnetite
of the eye and one below. This asymme- crystals is part of this system.
try apparently aids the vertical localization
of a sound. The wide head of the owl The endocrine glands
results in asynchronous arrival of sound
in the two ears and aids the owl’s ability Secretions of the endocrine glands are as
to pinpoint the direction from which integral to the coordination and proper
the sound originates. The owl will often functioning of the body as the nervous
rotate its head to maximize the difference system. Hormones secreted by these
in the arrival time and thus gain a “fix” on ductless glands are transported via the
the sound. Barn Owls also have very large circulatory system to all parts of the body,
eardrums, columellae, and cochleae, and where they effect changes in cellular
the region of the brain devoted to hearing processes. Their effects may be similar
is larger as well. As might be expected, to those caused by nerve stimulation,
the number of auditory neurons is much but they are much longer lasting. We
greater in a nocturnal hunter than in will briefly discuss some of the principal
a diurnal one.22 Barn Owls have about endocrine organs of the bird, along with
95,000 auditory neurons; the Carrion their hormones and actions. The gonads
Crow (Corvus corone) has only 27,000. (ovary and testis) are omitted here but are
chapter 2

The range of frequencies that can be covered later in the section on hormonal
heard at very low sound intensity is also control of reproduction.
greater in owls. Finally, once the owl has Pituitary. One of the most important of
determined the location of its prey, it flies the endocrine glands is the pituitary,

56

1stPages_A.indd 56 7/22/20 10:43 AM

 Fig. 2.21. Facial disk of a Barn Owl (Tyto mone (LH), gonadotropic hormones that
alba), which serves as a parabolic reflector stimulate the ovary and testis; somato-
to concentrate sound waves and direct them tropin, which stimulates growth in all
to the outer ears, which are behind the disk cells; and prolactin, which stimulates
and located very asymmetrically to assist with brooding behavior and the development
hearing. of the brood patch. The posterior lobe of
the pituitary is actually a downgrowth of
General Traits of an Avian Flying Machine
the brain and contains secretory neurons
which sits below the hypothalamus at the that manufacture oxytocin, which causes
base of the brain, supported by a slender expulsion of eggs from the oviduct, and
stalk of nerve tissue. The anterior lobe of arginine vasotocin, which acts as an
the pituitary consists of epithelial tissue antidiuretic (conserves water excretion
that secretes a variety of hormones that by the kidneys). Secretion of anterior
in turn stimulate other endocrine organs pituitary hormones is stimulated (or
and tissues of the body: thyroid-stimu- inhibited) by hypothalamic releasing
lating hormone (TSH), which stimulates factors; they are also regulated by nega-
the thyroid gland; adrenocorticotropic tive feedback from the products of their
hormone (ACTH), which stimulates target organs. Thus, increased levels of
the adrenal cortex; follicle-stimulating thyroid gland hormone (thyroxin) feed
hormone (FSH) and luteinizing hor- back to the pituitary and hypothalamus

57

1stPages_A.indd 57 7/22/20 10:43 AM

 to suppress the release of hypothalamic gen (in small amounts). The medulla
releasing factor (TSHRF) and pituitary secretes norepinephrine and epineph-
TSH. rine from nerve endings of sympathetic
Thyroid. The thyroid gland consists of fibers (the amounts of each vary greatly
paired, ovoid lobes found along the between species). The latter hormones
carotid arteries in the neck. The gland have profound and diverse effects on all
is composed of spherical follicles filled body organs in increasing heat produc-
with the secretory product, thyroxin, tion, fat catabolism, blood glucose, and
coupled to a globulin protein (thyro- heart rate and blood pressure. Medullary
globulin). Cells surrounding the folli- hormones produce a prolonged effect
cle sequester iodine from the blood to that is essentially the same as the short-
synthesize thyroxin, and the product is er-lasting sympathetic nervous system
then stored until levels of TSH cause its stimulation, a “fight-or-flight” response
release. Thyroxin increases the met- to stress.
abolic activity of all body cells and in Several factors influence the activity
the process causes an increase in heat of the adrenal gland. Some species show
production. It is necessary for normal an increase in adrenal activity in winter,
growth and development of the young, when glucocorticoids may aid thermo-
for gonadal growth, for feather growth, genesis (heat production) and main-
color, and structure, for migration (as tenance of high blood glucose levels.
a stimulator of nocturnal restlessness), Species of saltwater or saline habitats
and for overwintering (as a stimulator have enlarged adrenals and secrete more
of heat production and fat catabolism). mineralocorticoids. Species exposed
Thus, thyroid function is essential to chronic stress from crowded social
throughout the annual cycle: in repro- situations, harsh temperatures, or
duction, molt, migration, and winter disease (parasitism) also have enlarged
survival. adrenals. Pituitary ACTH acts only
Adrenal. The adrenal gland is also on the glucocorticoid-secreting cells;
referred to as the interrenal or supra- increases in the other cells are regu-
renal gland because of its location at lated by other factors, such as stress.
the anterior tip of the cranial lobe of Levels of corticosterone (one of the glu-
the kidneys. The gland consists of cocorticoids) exhibit a daily rhythm in
steroid-producing cells in the cortex birds that varies seasonally, and some
and sympathetic ganglion cells in the researchers suggest that this hormone
medulla. There is no zonation of cortical acts as a metabolic synchronizer for
tissue as in mammals; rather, the corti- the various events of the annual cycle.
cal and medullary tissues are intermin- For example, the temporal relation-
gled in the gland. However, the function ship between peaks of corticosterone
is essentially the same as in mammals. and prolactin in the plasma appears to
The cortex secretes glucocorticoids, determine whether the bird fattens or
chapter 2

which increase plasma levels of glucose; catabolizes fat, migrates north or south,
mineralocorticoids, which increase exhibits nocturnal restlessness, or
electrolyte reabsorption in the kidneys; exhibits gonadal growth or regression
and the sex steroids androgen and estro- (see the section on photoperiod control

58

1stPages_A.indd 58 7/22/20 10:43 AM

 of reproduction in chapter 11). metabolism. Calcium ions are involved
Pancreas. The pancreas lies in the in many functions in the bird: muscle
duodenal loop and has both exocrine contraction, membrane permeability, cal-
(enzyme secretion via ducts) and endo- cification of bone and eggshell, clotting of
crine functions (see the section above on blood, and as an enzymatic cofactor. Para-
digestion). The endocrine products are thormone causes the release of calcium
secreted by the cells in the islets of Lang- from the skeletal reservoir and increases
erhans, which make up less than 1% its reabsorption in the kidneys and gut. It
of the total pancreatic tissue. Four cell acts synergistically with estrogen during
types produce four distinct hormones: the laying cycle and causes hypercal-
glucagon, which raises blood glucose; cemia, which ensures that sufficient
insulin, which lowers both blood glu- calcium is present for eggshell synthesis.
cose and blood fatty acids by increasing Levels of parathormone are regulated by
cellular uptake; pancreatic polypeptide, the feedback action of plasma calcium
which depresses gastric motility and levels on the parathyroids, but the action
secretion in some species; and soma- of the hormone is opposed by the secre-
tostatin, a growth hormone inhibitory tion from the ultimobranchial bodies
factor. Control of insulin and glucagon (just posterior to the thyroid gland) of
secretion is independent of the pituitary calcitonin, a hypocalcemic hormone.
and is instead affected by levels of blood Other endocrine tissues. Other hormones
glucose, as in mammals; that is, high are secreted at other locations through-
blood glucose stimulates insulin release, out the body. In young birds the thymus,
whereas low blood glucose stimulates which lies along either jugular in the
glucagon release. However, there are neck, and the bursa of Fabricius, found
some important differences between on the dorsal surface of the cloaca, secrete
birds and mammals in response to hormones that are important in the mat-
these two hormones. Birds have many uration of certain types of lymphocytes.
more glucagon-secreting cells and 5 to Secretin and cholecystokinin secreted
10 times more glucagon in the pancreas by specialized cells in the duodenum
than mammals, and avian glucagon regulate the release of watery bicarbonate
is more potent in producing elevated buffer and pancreatic enzymes and bile,
General Traits of an Avian Flying Machine
blood glucose than the mammalian respectively. Gastrin secreted by cells in
hormone. In addition, not only do birds the glandular stomach regulates the acid
have fewer insulin-secreting cells in the production of other cells in the glandular
pancreas, but they are about 500 times stomach. Neuropeptides (proteins ini-
less sensitive to it than mammals. This tially found in the brain) have now been
may explain why birds typically have found in many peripheral tissues, and
much higher blood glucose levels than their role there has yet to be discovered.
mammals. Endocrine function is comprehensive and
Parathyroid. Two parathyroid glands are complex, and through this system, birds
found near the posterior margin of each possess fine-tuned control of long-term
thyroid gland. There is only one type of processes.
cell in the parathyroid, and it secretes
parathormone, which regulates calcium

59

1stPages_A.indd 59 7/22/20 10:43 AM

 Fig. 2.22. Metabolic rate (per
animal) as a function of body
size in different vertebrate
groups. From Bartholomew
(1977).

Energy Metabolism 10% of the total time budget.

Birds are endothermic, which
The lifestyle of birds is very energy means they maintain a high, constant
demanding, and birds possess the high- body temperature, in this case by means
est rates of resting and active metab- of internal heat production from shiv-
olism among vertebrates (fig. 2.22). ering activity of muscles. As with all
Passerine metabolic rates are roughly endotherms, the energy expended to
twice that of a mammal of the same maintain a constant body temperature
size and more than 10 times that of a is a function of the thermal gradient
similar-sized reptile. This is not simply between environmental temperature
because of their expensive mode of loco- and body temperature and the sur-
motion. As discussed earlier, the met- face-to-volume ratio of the bird. In
abolic cost of flight is 9–12 times that general, the steeper the thermal gradient
of resting in small passerines; however, between core and surface temperatures,
most birds do not fly continuously all the greater the potential for heat loss or
chapter 2

day. In fact, the time spent flying may be gain at the surface, and consequently
as little as 2% of the total daily activity in in the core as well (fig. 2.23). Within a
Bald Eagles (Haliaeetus leucocephalus).24 certain range of environmental tem-
In most birds, flight time may be only perature, the heat loss or gain can be

60

1stPages_A.indd 60 7/22/20 10:44 AM

 offset by changing the insulation or by Fig. 2.23. Metabolic rates expressed as a
postural changes, that is, fluffing feath- percentage of basal (resting) metabolism for a
ers or retracting extremities to conserve large bird (a ptarmigan, 326 g) and a crowned
heat, and sleeking feathers or exposing sparrow (29 g) at different temperatures. The
extremities to facilitate heat loss. This thermoneutral zone (TNZ) is determined by
range of environmental temperatures the size-dependent lower critical temperature
is called the thermoneutral zone (TNZ). (Tlc) and upper critical temperature (Tuc)
for a bird. The TNZ includes those conditions
Below the TNZ, heat must be produced
where basal metabolism is relatively constant.
by shivering to offset heat loss from the
It includes lower temperatures for the larger
surface. Thus, the energy expended to
General Traits of an Avian Flying Machine
ptarmigan, which also has a larger TNZ than
thermoregulate increases with decreas- the sparrow. Because bird body temperature
ing environmental temperatures. is so high, the size of the bird is less important
Likewise, above the TNZ the bird gains when temperature exceeds the TNZ
heat from the environment that it must (Bartholomew 1977).
dissipate by evaporation. This is also an
active process that requires some meta-
bolic investment. Thus, at environmen- than 1000 g (roughly 2 pounds). Small
tal temperatures both above and below animals have a larger surface area for
thermoneutrality, birds must expend heat loss compared to their heat-produc-
energy to maintain a constant core tem- ing volume than large ones. Hence, on a
perature. per gram basis, metabolism is higher in
Birds also tend to be fairly small, with small birds than in larger ones (fig. 2.22).
most of the 10,000 species being less In addition, small birds must respond

61

1stPages_A.indd 61 7/22/20 10:44 AM

 more quickly and more intensely to middle of winter) than species living
changes in environmental temperature, at more southerly latitudes. The addi-
because of their smaller heat reservoir. tional cost of existence in a cold climate
The greater rate of heat loss from a small is due primarily to the energy required
body necessitates a higher rate of metab- for thermoregulation and, to a lesser
olism to maintain a constant core tem- extent, to the increased activity required
perature (fig. 2.23), although the fact that to find food in a less productive area.
normal bird temperatures are so close to For example, it has been calculated that
the thermal maximum means that birds House Sparrows (Passer domesticus)
of all sizes respond fairly similarly when expended 39% more energy daily during
above the TNZ. the winter than in the summer.25 In
We noted earlier that energy require- addition, added costs are incurred at cer-
ments for existence are higher in birds tain times in the annual cycle because
than in any other vertebrate group. of molt, migration, and reproduction.
This might be explained by the gener- Annual variation in daily energy expen-
ally small size of birds; however, avian ditures has been documented for some
energy requirements are higher than species—for example, the Black-billed
those of mammals, for example, even in Magpie (Pica pica)26 and the House
similar-sized species of the two classes. Sparrow (fig. 2.24).27 Daily expenditures
The reason for this is largely that birds range from a low of 1.3 times resting
regulate higher body temperatures than metabolism (metabolism measured
mammals (40°–41°C in birds, 37°–38°C during the inactive period at thermoneu-
in mammals) and consequently main- tral temperatures) in incubating birds
tain steeper core-to-surface temperature to 5–7 times resting metabolism during
gradients. In light of this relationship the severe weather of midwinter. Gen-
between level of core temperature erally, the average daily metabolic rate
regulated and metabolic expense, it is increases with the amount of time spent
interesting to note that passerine birds flying and depends strongly on changes
have higher metabolic rates (and higher in environmental tem­perature.
body temperatures) than nonpasserines To meet their high energy demands,
of similar size (fig. 2.22). birds specialize on high-energy foods
Several other factors can affect the such as insects, fruits, seeds, and other
energy requirements of birds. There are vertebrates. On these diets birds can
differences in metabolism between day assimilate more than 75% of the food
and night, which reflect activity level. energy, compared to only 30% of the
For example, diurnal metabolism of energy in plant matter other than fruits
day-active caged birds is 1.2–1.4 times and seeds. The need for high-energy food
the nocturnal resting metabolism, which is most pronounced in the smallest birds.
may simply reflect the birds’ greater Thus, it is not surprising that the smallest
muscle tone and alertness during the birds in the world (hummingbirds) are
chapter 2

daytime. Climatic factors also contribute specialized to feed on nectar, a high-oc-

greatly to energy demands; northern-­ tane fuel that is almost pure sugar, and
latitude species have much greater may supplement their diet with insects
energy requirements (especially in the when nectar is scarce. Even in moder-

62

1stPages_A.indd 62 7/22/20 10:44 AM

 Fig. 2.24. Variation in
daily energy expenditure
for House Sparrows
(Passer domesticus)
in Illinois through the
year. Basal metabolism
(purple) varies seasonally,
as does the amount of
energy allocated to body
temperature regulation
(blue). Caged or flight
movement costs are
shown in green and
olive. Energetic costs of
reproduction are shown in
beige, while those of molt
are in crosshatched brown.
From Kendeigh, Dol’nik,
and Gavrilkov (1977).

ately cold weather when air temperatures energy demands exceed the bird’s meta-
just reach the freezing point, the energy bolic fuel supply, in some cases the bird
General Traits of an Avian Flying Machine
demands placed on small insectivores may lower its body temperature slightly
(< 10 g) are such that they must eat or go into torpor to conserve energy until
50%–75% of their own body weight in the morning feeding period (see chapter
food each day. For example, 12 g Black- 8). There is a distinct disadvantage to
capped Chickadees (Poecile atricapillus) being small: the amount of metabolic
held in captivity at freezing temperatures fuel that can be stored is also small, and
ate 9 g of insects per day to maintain fasting tolerance is very low.
their body weight. There is a size at Large-bodied birds can store much
which a bird simply cannot eat or process greater amounts of fat and can with-
food fast enough to avoid starvation. In stand long periods of food deprivation.
birds, the lower limit appears to be about For example, the male Emperor Penguin
2 g, the approximate weight of the Bee (Aptenodytes forsteri) endures a fast of
Hummingbird (Mellisuga helenae). When over 100 days while it makes its way

63

1stPages_A.indd 63 7/22/20 10:44 AM

 across the sea ice to breed, incubates its 17 kg, and is a grazing herbivore rather
egg, feeds its chick for a short time after than a carnivore or scavenger. Fossils of
it hatches, and returns to the sea. The a Pleistocene condor, Teratornis incred-
limitations to large size are also affected ibilis, suggest this bird weighed up to
by the quality and quantity of food and 20 kg, but fossils from North Carolina
to a greater extent by the energetic costs have recently been described as an alba-
associated with finding and procuring tross-like seabird that had a wingspan of
the food. While a large bird is metabol- 6.4 m and may have weighted up to 40
ically efficient on a per gram basis, the kg.28 For these species to fly, they must
actual amount of food needed to survive have lived in exceptionally windy envi-
daily increases with body size to a point, ronments. Of course, nonfliers can be
as in small birds, where energy cannot even larger than these and can survive
be harvested fast enough. It is not sur- on lower-quality food, such as various
prising that the largest flying birds are plant materials.
carnivores and scavengers (e.g., eagles, In the following chapter we will deal
vultures) that feed on high-energy foods further with the energetic cost of flight,
that can be obtained in large pieces. and in later chapters we will deal with
Empirical calculations of the maximum foods and food gathering. At this point,
weight compatible with horizontal we must simply appreciate that the avian
flapping flight estimate this weight body is a high-intensity machine that
at 12 kg. However, the heaviest extant requires a great quantity of energy to
flying bird, the Whooper Swan (Cygnus sustain it.
cygnus), is even larger than this, about
chapter 2

64

1stPages_A.indd 64 7/22/20 10:44 AM

 C HA P T E R 3

Flight

I
n chapter 1, we suggested two Gliding
alternative hypotheses of how birds
developed flight. The arboreal In both hypotheses for the evolution
theory envisions some preavian of flight, we can envision a creature
reptile that developed the ability to surrounded by a current of moving air
climb trees and glide down from them while fighting the earthward pull of
to capture prey, escape from predators, gravity by extending some form of early
or travel. The cursorial theory suggests wing outward from the body. The goal
that in some bipedal lizards of open of an efficient glider is to counteract
country, the forelimbs became modified the effects of gravity enough that many
to provide lift and thus made running units of horizontal distance are gained
an energetically less expensive move- for each unit of vertical distance lost.
ment. In both cases, the chief elements The first step would be the development
working to defeat the effects of gravity of a new surface to increase the area of
were the hind legs, while the forelegs interaction between the animal and the
were modified either to provide lift for a air. Some present-day gliding animals
terrestrial running bird or to extend and achieve this increased area by develop-
control the fall of an arboreal proavis. ing skin between the forelegs and hind
For this reason, we begin this legs, as in flying squirrels and some glid-
chapter by examining the aerodynamic ing lizards. Gliding snakes accentuate
guidelines that shape a bird into an effi- the spread of their bodies to accomplish
cient glider. To this basic glider model, the same purpose. Since primitive birds
we will later add the mechanisms to apparently needed their hind legs to be
promote powered flight. Different types free for climbing ​or running, the obvi-
of birds have adopted different balances ous place for them to develop a large
between the adaptations for gliding and surface was on the forelimb (although
those for powered flight, and we exam- we have seen recent fossils with feathers
ine the major types of flying techniques on both wings and legs).
in birds. We end by taking a look at the Given that there developed a prim-
birds that could at some point in their itive bird (or modified lizard or dino-
history fly but are now flightless. saur) with a wing of some sort, we need
to understand how various surfaces
move through the air to understand the
forces shaping the wing. To begin with,
we must remember that the air exerts

65

1stPages_A.indd 65 7/22/20 10:44 AM

 pressure in all directions, much as water reduces the air pressure above the wing
does but with less force. A motionless relative to that below it and therefore can
object hanging in the air is pushed in cause lift. Increasing the amount of tilt
all directions by the air with the same of this plane relative to wind direction
force. Next, we must be aware that air (termed the angle of attack) increases
pressure varies with air speed; as air the difference between the distances air
speed increases, the pressure that air must travel above and below the wing
can exert on a surface is reduced. If an and thus increases potential lift. With
object has motionless air on one side of this simple plane, however, it takes
it and moving air on the other side, the only a small change in angle of attack
pressure on the motionless side will be to destroy any lifting properties. This is
greater than that on the moving side. If because turbulence develops rapidly as
this pressure difference is great enough, the angle of attack is increased; this tur-
it can cause the object to move. This can bulence amounts to swirling of the air
be shown by holding a piece of paper by behind the wing, which tends to reduce
the two near corners and blowing across air speed and thus to increase pressure.
the top of it. While you might expect This reduces the differential pressure
the paper to move away from the mov- between the top and bottom of the plane
ing air because of the pushing effect of and negates any lift, a situation known
such movement, in fact, the paper will as a stall.
rise, because the pressure from below is Although a simple plane can cause
greater than the pressure on top of the lift and flight, particularly if properly
paper when the air is moving. outfitted with a tail apparatus, it is very
If our primitive wing were a simple inefficient because stalls can occur so
geometric plane, with length and width easily. Also, with a rigid plane for a
but very thin, it could cut through a wing, the only flexibility in movement
moving airstream with little resistance is with the limited allowable changes in
and with little effect on the air if it were the angle of attack. To improve on this
positioned such that one of the long axes basic plan, the avian wing has devel-
of the plane were parallel to the wind oped into an airfoil that is much more
direction (fig. 3.1). If we tilt this plane sophisticated than a simple geometric
ever so slightly, such that the leading plane (fig. 3.1). While the leading edge
edge of the plane is higher (relative to formed by a strip of skin called the pata-
the airflow) than the trailing edge, sev- gium allows a flexible surface that cuts
eral things happen. First, the airstream through the air like a knife, the wing
that hits the leading edge of the wing rather quickly thickens and then more
splits and moves around the plane to gradually tapers off. The wing also has a
re-form beyond it. Because the air that generally curved shape, and the amount
goes under the wing has slightly less of curvature (called the camber) is also
distance to travel than the air going over variable. This aerodynamic streamlin-
the wing before the airflows meet again, ing of our initial plane maximizes the
chapter 3

the air above the wing moves more potential difference in the distances air
rapidly than that below it. This generally must travel over and under the wing (to
faster movement of air above the plane maximize the relative pressure differ-

66

1stPages_A.indd 66 7/22/20 10:44 AM

 Fig. 3.1. Variation in lift provided by a simple of attack or by changing the camber (cur-
geometric plane (top) or an airfoil (bottom) vature) of the wing. Too much of an adjust-
under different air conditions. At upper left, ment in angle of attack or camber will still
the plane is parallel to the wind direction break up the smooth flow of air and cause
and thin enough that no effect on the wind a stall, but this problem can be reduced
occurs. If the plane is tilted, the airstream by the addition of a slot above the airfoil
is split, and air moving over the plane must
(fig. 3.1). This slot forces air down across
move faster to catch up with the airflow at
the upper wing surface, thereby reducing
the back of the plane. The difference in speed
stalls when either the camber or angle of
reduces air pressure above the wing and may
provide lift. Too much tilt into the wind (too attack is large. The alula creates this slot
great of an angle of attack) causes turbulence above the airfoil formed by the secondary
above and behind the wing, which destroys feathers in a bird; it is particularly import-
lift and causes a stall. In the airfoil, the shape ant during takeoffs and landings, when the
smooths out the movement of air to maximize slow speed of the bird reduces lift and the
lift (bottom left), but too great an angle of required posture of the bird may put the
attack can cause stall conditions (middle). angle of attack in stall position (fig. 3.2).
The stall conditions can be remedied by use Slotting also occurs among those primary
of a slot above the wing (bottom right). This feathers that tend to extend beyond the
slot (formed by the alula in birds) forces air solid portion of the wing (see below); each
down along the upper wing surface, reducing
primary serves as a tiny airfoil in shape,
turbulence and stalling.
but the occurrence of a row of primaries
results in their serving as slots for one
another. These slotted primaries can also
ence) while it minimizes the turbulence reduce stalling by providing lift from the
of air passing over the wing. primary feathers even when the secondar-
This three-dimensional airfoil is ies are in stall position (fig. 3.2).
much more effective at causing lift than Even though we can think of the
a two-dimensional one. It also has more development of the aerodynamic avian
flexibility with changing air conditions. It wing as a gliding tool, the same principles
Flight

can increase lift by increasing the angle of lift relative to airflow apply to powered

67

1stPages_A.indd 67 7/22/20 10:44 AM

 flight. The difference is that in powered Fig. 3.2. Landing in a Harris’s Hawk
flight, the movement of the bird through (Parabuteo unicinctus) is simply a controlled
the air is caused by its own efforts. In stall. The bird shifts its body position to a
this situation, secondaries usually act as more upright posture, which causes stalling
full-time gliders to provide continuous conditions across the airfoil made by the wings
lift, while other parts of the wing provide and spread tail feathers. This stall is controlled
by the spread tail and the alula of each wing.
the necessary forward motion that keeps
The separated primaries may also provide lift
air moving around the wing.
to control the stalling.

Powered Flight

All the aerodynamic properties of a obvious location for modification into a

glider are worthless without a flow of source of power was the forelimb, which
air over the wing. If the first avian glider by this time may have already been
was an arboreal lizard, no matter how turned into a gliding apparatus. As we
efficient a glider it was, it periodically pointed out earlier, the avian paleonto-
had to climb a tree to be in a position to logical story is too sketchy at this time to
create airflow. An open-country, terres- say how the development of gliding and
trial glider would have to run rapidly to powered flight really occurred. While
create the same airflow on a windless gliding seems to have been a necessary
day. Thus, once primitive gliding ability first step, even primitive gliders may
was developed, the next step was the have initiated the development of pow-
chapter 3

production of a source of power that ered flight. With limited fossils, we are
negated the need to climb or run. Since more or less forced to examine modern
the hind limbs were needed as legs, the forms of powered fliers.

68

1stPages_A.indd 68 7/22/20 10:44 AM

 In modern birds, forward momen- This feather arrangement gives a
tum is provided by the movement of high-resistance downstroke and a low-re-
the primary feathers of the wing. Thus, sistance upstroke, which is correlated
while the secondaries of a bird wing with the size of the pectoral muscles
provide lift much as an airplane wing doing the pulling on these strokes. But
does, the primaries of the wing provide birds do not generally flap up and down,
power in the manner of an airplane pro- nor do they pull at the air in the manner
peller. The structure and position of each of a human swimmer. Rather, birds use
primary feather are critical to this action the pectoral muscles to pull the wings
(fig. 3.3). All primaries are attached to the down and forward to the bottom of the
fused hand bones (termed the manus, stroke. The primaries are then pulled
see fig. 2.11), allowing great flexibility of back and upward to the peak of the
movement. Most primaries, and partic- stroke, which has sketched either a tilted
ularly those nearest the leading edge of oval or sometimes a figure eight (fig.
the wing, are asymmetrical in structure, 3.4). In all birds but hummingbirds, the
giving them the general shape of minia- stroke down and forward provides the
ture airfoils to provide lift (fig. 3.3). These power, while the stroke up and backward
feathers are also quite flexible, allowing is designed for minimal resistance.
movement in response to air pressure. As the primaries are providing
Thus, with a downward motion of the this power, the secondaries are trav-
wing, air pressure pushes the large area eling through the air doing their job
of the trailing edge of each flight feather
against the shaft of the primary behind
it. This effectively closes the wing to Fig. 3.3. Interaction of the primary feathers
make a solid surface impermeable to air during the power stroke as seen in a cross-
(fig. 3.3). In contrast, upward movement sectional view. When moving through the air
(top left), each primary may act as an airfoil
of the wing causes air pressure to twist
and provide lift. But when the wing is moving
the feather away from the other prima-
downward, the primaries close so that no
ries such that air passes through the
air can move through the wing (left middle)
wing like light through an open venetian except where slots occur on the outer primaries.
blind. It has been estimated that the On the upstroke (right) the primaries open
resistance to the upstroke is about 1/10 such that there is little resistance on the
that to the downstroke. upstroke.
Flight

69

1stPages_A.indd 69 7/22/20 10:45 AM

 Fig. 3.4. Movement of the wing on a
of providing lift. The flexibility of the
typical power stroke in a Mallard (Anas
manus allows the primaries to move in platyrhynchos). Note that on the downstroke,
a large arc even while the secondaries the wing often twists such that the air pushed
are relatively level (fig. 3.4). To visualize by the stroke moves backward as much as
this, grab a yardstick in your hands, downward (Wilson 1980).
stick your arms straight out, and swing
your arms in an oval arc, moving your
elbows only a few inches but rotating posture, meaning that the angle of nor-
your hands as much as possible. Note mal flapping in flight is initially an angle
the size of the circle made by the end of of attack that would produce a stall. To
the yardstick. While this does not exactly overcome this, the bird usually takes
mimic a bird’s flap, you can see how the off into the wind and launches itself
primaries (the yardstick) are moving a with a powerful thrust of its legs. This
great distance while the lift-generating may allow it to get far enough from the
surfaces are relatively stationary. While ground or a perch to flap freely and shift
you have your yardstick out, tape a piece its body position to one more appropri-
of cardboard to it and note how move- ate for flight. The first wing beats are in
ment through the wing stroke twists the very large arcs (if you flush a pigeon you
yardstick. Think about how this twist- can hear the wing tips hit one another
ing would occur if the yardstick were on the first few flaps), with the ovals
a feather with neighboring feathers. described by the strokes relatively hori-
This twisting (called pitch) can turn the zontal. The alula is very important here,
whole wing or each feather tip (in slotted because it forces air across the wing
wings) into a variable pitch propeller during the first flaps when the angle
that provides the power for a flying bird. of attack of the wing is at or beyond its
stalling point. If you remove the alula,
Takeoffs, Landings, and some birds cannot take off. During the
Aerial Maneuvers first flaps, the primaries are as separated
as they can be, maximizing the slotting
Before the system of propulsion and lift effect that allows each primary to act as
described above can work, the bird must an airfoil and provide maximum lift.
get off the ground and develop a flow For most species, this process of
of air over the wings. In addition to the jumping and flapping is not difficult,
chapter 3

large inertia that must be overcome, a but the general body design of others
perched or standing bird often has a pos- has made taking off a problem. Many
ture that is more upright than the flying diving birds such as loons and grebes

70

1stPages_A.indd 70 7/22/20 10:45 AM

 have their feet placed at the extreme rear effective air brakes in addition to being
of their bodies to aid in underwater pro- good paddles. Some African vultures,
pulsion. To take off from water, the bird which never paddle in water, have small
must throw its body forward and paddle webs on their feet to help them slow
across the surface of the water while down when swooping at great speeds
beating its wings until it gains enough from high in the sky. Species such as
speed and lift to fly. Some waterbirds frigatebirds with very long, skinny wings
can barely shuffle on land and cannot may have deeply forked tails that can be
take off from there. Albatrosses and a spread very wide. When this is done, it
few others can take off only by running greatly increases the size of the airfoil
into the wind until they gain enough formed by the wings and tail and thus
speed. Because of these problems, alba- aids in braking.
tross nesting colonies are nearly always The tail also serves a critical function
on the windward sides of islands with in maneuvering. It does this in much
either cliffs from which the birds can the same way it helps with braking, but
jump into the wind or open areas such it drops only partially to cause resistance
as beaches where they can run. on one side to help turn the bird (much
Landing presents the opposite in the manner of a rudder on a boat). Of
problems, with a bird trying to counter course, if the maneuvers are extreme,
all the momentum it has developed. One tail position shifts are also aided by vari-
of the first things it does is increase the ation in the shape of each wing to effect
angle of attack of the wings to the point the change in direction.
of stalling. The air turbulence produced Although our description suggests
breaks the forward momentum, as does that the major activities involved in
beating the primaries more or less hori- flight are rather simple, it should be kept
zontally against the flow of air. The tail is in mind that coordinating all the various
very important in landing. Although we activities involved in flying is anything
consider the secondaries to be the prime but a simple task. Each flap requires a
airfoils that provide lift, the body and tremendous synchrony of action plus
tail also serve as an airfoil. When the tail a continuous monitoring of both the
is spread and dropped, this makes the position of the bird and the relative flow
whole body an airfoil with an angle of of air around it. Although composed of
attack great enough to cause strong tur- fairly simple components, the total pack-
bulence and stalling conditions (see fig. age of flying is incredibly complex.
3.2). It is not surprising that birds whose
lifestyles require highly maneuverable Variations in Flying Technique
flight often have long and sometimes
broad tails for good control of braking As we will see in more detail later, birds
and other maneuvers. Species with short inhabit virtually all regions of the earth
tails, in particular many of the diving and feed on a variety of foods that they
birds that have such difficulty taking catch in many different ways. The result
off, may hang their feet to increase air is that birds must deal with a variety of
resistance and aid braking. When these wind conditions in their lives. Thus, it is
Flight

feet are large and webbed, they are very not surprising that great variations occur

71

1stPages_A.indd 71 7/22/20 10:45 AM

 in the general design of flying birds. tum. Wing loading varies with size in
We have pointed out that the avian quite interesting ways. Because surface
wing is part glider (the secondaries) and increases as the square of a linear mea-
part propeller (the primaries). While sure and because weight increases as
all flying birds must have both, most of the cube of length, doubling the length
the variation in the shape of the wing, of a bird squares the surface of the wing
and consequently in the type of flight, but cubes the bird’s weight. Obviously,
reflects the extent to which gliding flight this greatly reduces the wing loading of
is developed relative to powered flight. the bird (fig. 3.5). It is relatively easy for
The balance between these two mech- small birds to have wings big enough
anisms is related to the availability of to support their weight, but the above
external sources of air movement and relationship poses severe hardships for
the lifestyle of the bird. Two major phe- larger birds. For example, if a goose
nomena help explain how and why these were to have the same wing loading as
changes in wing shape are adaptive: most small birds, its wings would need
tip vortex and wing loading. Tip vortex to have nearly 10 times the area they
refers to the turbulence that occurs at actually have. Such wings are impossible
the tip of the wing because of distur- both physiologically and mechanically.
bance of air by the moving bird. While This means that larger birds are work-
wing shape and the alula can reduce air ing with less margin of error regarding
turbulence over and behind the wing, wing loading. Although this may be
there will always be some tip vortex that compensated somewhat by the reduced
causes drag. The effect of tip vortex can tip vortex of large wings, wing loading
be reduced, though, by increasing the determines the ultimate size limits of
aspect ratio, which is the ratio of wing flying birds and puts severe constraints
length to width. Because the tip vortex on nearly all large fliers.
stays constant as wing width stays con-
stant, increasing wing length increases Wing types
the area providing lift and therefore
increases the lift-to-drag ratio (since Given the above mechanical constraints
drag stays constant). This suggests that and the possible variation in the places
a species living in a situation where it where birds live and the ways they feed,
must try to maximize its gliding abilities every wing type imaginable occurs.
should have relatively long, thin wings These have generally been divided into
compared to species that are primarily four categories (fig. 3.6): (1) elliptical
self-powered fliers. wing, (2) high-speed wing, (3) high-as-
The second aerodynamic factor that pect-ratio wing, and (4) slotted high-lift
affects wing shape variation is wing wing—but we also suggest that there
loading (also called wing disc loading), should be a fifth category, the super-
the ratio of wing area to weight. Obvi- high-speed wing.
ously, this is important because the wing Elliptical wing. The elliptical wing is the
chapter 3

area must be large enough to provide most typical bird wing. It has a relatively
both lift to carry the weight of the flying low aspect ratio but a high amount of
bird and the necessary forward momen- slotting of the primary feathers. The

72

1stPages_A.indd 72 7/22/20 10:45 AM

 Fig. 3.5. Relationship
between wing area (vertical
axis) in square centimeters
and body weight (horizontal
axis) in grams in birds.
Because bird weight
increases more rapidly than
wing area, there is a limit to
how large flying birds can be
(Wilson 1980).

Fig. 3.6. Five categories of wing type, showing

the relative proportions of primaries (orange),
Flight

secondaries (yellow), and slotting (red) (Savile

1957).

73

1stPages_A.indd 73 7/22/20 10:46 AM

 flight produced is relatively slow but very the primaries. It generally has a high
maneuverable, although much variation aspect ratio, low camber (curvature), and
occurs within this group (fig. 3.7). For a swept-back look (fig. 3.6). It occurs
example, chicken-like birds have very in a variety of birds that feed in the air
rounded wings that are used for quick (swifts, hummingbirds, terns, falcons,
bursts to elude predators, while migra- and swallows) and in some that undergo
tory birds have relatively pointed wings long migrations (ducks, shorebirds).
to reduce wing loading and tip vortex Species with high-speed wings must flap
during long flights. Other birds with
generally elliptical wings include doves,
Fig. 3.7. The wide variation in avian wing types
woodpeckers, and most songbirds. with respect to body size, aspect ratio, and
High-speed wing. The high-speed wing amount of slotting. These are not necessarily
forms only one airfoil from base to tip all in the proper position relative to one
because it tapers with no slotting of another (Savile 1957).
chapter 3

74

1stPages_A.indd 74 7/22/20 10:46 AM

 nearly continuously, which makes this one the often heavy-bodied bird glides down-
of the most energetically expensive forms ward with the wind to develop momen-
of flying. tum. Near the water surface, it turns into
High-aspect-ratio wing. The high-as- the wind, using the lift developed by its
pect-ratio wing is similar to the high- long wings to rise. Because the winds are
speed wing in being long and narrow and stronger as the bird rises, more and more
unslotted, but it is much longer because lift is developed until the bird decides to
of an elongated humerus (fig. 3.6). This turn and glide downward again. Although
results in a longer area of secondary feath- this type of soaring can be used in some
ers for lift and occurs primarily in a few instances over land, true dynamic soarers
species of oceanic seabirds that practice are primarily oceanic and usually confined
what is known as dynamic soaring (fig. to the windier parts of the world.
3.8). This form of soaring utilizes varia- Slotted high-lift wing. Although often
tion in wind velocities that is associated relatively long, the slotted high-lift wing
with wave action. Therefore, it is some- has a moderate aspect ratio because it is
times called wind gradient soaring. Mov- also quite wide and has a deep camber.
ing air over the ocean surface causes wave It also has very pronounced slotting,
formation and, in the process, is slowed
relative to air higher above the water. A Fig. 3.8. An albatross and how it uses dynamic
bird using dynamic soaring works in a soaring to move across the ocean surface
series of loops. From the peak of a loop, (Pennycuick 1975).

75

1stPages_A.indd 75 7/22/20 10:47 AM

 which is best displayed by hawks and Fig. 3.9. A condor and how it uses static
vultures that use what is called static soaring to move across land.
soaring. Static soaring takes advantage
of large and usually high-elevation air loops of an oceanic dynamic soarer.
disturbances. These may be the result Migratory storks of Europe and Asia use
of the upward deflection of air currents this method to travel between their win-
by slopes or obstructions, or they may tering grounds and breeding grounds, a
take the form of thermals, rapidly rising practice that is estimated to reduce fuel
pockets of air caused by the uneven consumption by a factor of more than
heating of the earth’s surface (fig. 3.9).1 20 over powered flight.2 The advantage
A static soarer uses the lift provided by of the large, slotted, high-lift wings to
the deeply slotted, high-camber wings such large birds is shown by the esti-
and the upward movement of air to mate that a warbler attempting to travel
almost effortlessly gain altitude, usu- in the same manner would reduce its
ally by circling within the rising air. fuel consumption by a factor of only 2.
These slots may form nearly 40% of Super-high-speed wing. Swifts and hum-
the wingspan of large soarers such as mingbirds have wings that are mostly
condors (fig. 3.9). This great lift allows primaries, with few secondaries (fig.
these large, heavy-bodied birds to soar 3.10). Such a design on small-bodied
in slow-moving air masses while main- birds provides for high speed but at a
taining high maneuverability. Once a high energetic cost because little lift is
high altitude has been gained, the bird provided by the secondaries. As we will
can glide wherever it wants. Migratory see later, the reduction of bones in hum-
static soarers or wide-ranging foragers mingbirds allows them to be exception-
chapter 3

will climb in one thermal and then glide ally flexible in how they can fly.
to the next. This creates a series of loops, Although it has generally been
but on a much grander scale than the suggested that static soaring occurs over

76

1stPages_A.indd 76 7/22/20 10:47 AM

 Harrier wings are somewhat longer
than those of other raptors, with most
Fig. 3.10. The shortening of the bones in a
of the increased length occurring in the
hummingbird allows it to rotate its shoulder
secondaries. A variety of frigatebirds
and flap its wings in nearly all directions, which
means it can move forward, backward, or (Fregata) occur in tropical oceans of the
hover in place (below) (Johnsgard 1983). world and are distinctive for having
the lowest wing loading of any bird.3
Although frigates use dynamic soaring
land and dynamic soaring occurs over when actively foraging on the ocean sur-
water, this is not always the case. In face, they regularly make long-distance
open grasslands such as the Great Plains movements by rising in thermals as
of the United States, raptors such as the clouds are formed by heating the ocean.
Northern Harrier (Circus cyaneus) hunt A frigate can rise at 4 to 5 m per second
for rodents by flying just above the grass and go as high as 4100 m; this allows
and taking advantage of the turbulence it to glide up to 60 km, as it searches
Flight

caused by wind blowing on the grass. for another forming cloud to repeat the

77

1stPages_A.indd 77 7/22/20 10:47 AM

 process. Some frigates flew continuously resting period during which the bird
for as much as two months; one juvenile falls. This roller-coaster pattern presum-
went as far as 55,000 km in 185 days, ably helps the bird save some energy
with only 4 days of rest on land during while flying. This same principle has
that time. been used to explain why birds such as
geese fly in a V or line formation. It has
Hovering been suggested that formation flying
reduces the energy lost to the resistance
Some variations in bird flight are not as of cutting through the air and allows
correlated with variation in wing shape. birds to gain additional lift from the air
Birds with all wing types will occasionally turbulence caused by the bird beside
hover, although this behavior is energeti- and ahead of them.4 Others have argued,
cally expensive. Hovering is done by flex- however, that these formations are the
ing the wings in such a way that both for- result of social interactions within a
ward and downward motion are negated flock and have little to do with the mech-
by wind speed and lift. The most accom- anisms of flight or energy reduction. In
plished hoverers are birds with elliptical any case, soaring birds optimize their
or high-speed wings, and the epitome of morphological adaptations by being very
hovering occurs in hummingbirds. These good at recognizing the location of ther-
tiny birds feed by hovering in front of mals or other updrafts. Most long-dis-
flowers and extracting nectar with their tance fliers have ways of timing their
tongues. Their high-powered wing is flights to coincide with favorable wind
unusual in being constructed with very conditions. We will show in more detail
short arm bones (humerus, radius, and in chapter 9 how migratory schedules
ulna) and longer hand bones (fig. 3.10). and routes often reflect seasonal shifts
These act much as a single bone, but the in prevailing winds or the movement of
whole shoulder is able to rotate, thereby pressure cells.
forming a variable pitch propeller that Although birds employ a variety of
can push air in nearly any direction on techniques to cut the costs of flying, at
both forward and backward strokes (fig. some point on a gradient of increasing
3.10). Not only can a hummingbird hover bird size, flight becomes too costly.
by beating its wings in a horizontal plane Where this occurs depends in part on
with equal power on both strokes; it can the type of wing and flight involved and
rotate these wings even farther so that it the foods available to a particular bird.
can fly backward. The extremely rapid flight of hum-
mingbirds with its extensive amount
Energy-saving flight behavior of hovering has a great energetic cost.
Hummingbirds seem to be success-
Birds use a variety of behaviors to try ful despite this cost for three reasons.
to reduce the energetic costs of flying. First, hummingbirds are small, thereby
Woodpeckers are among a small group reducing the work required to hold
chapter 3

of birds that exhibit undulating flight, themselves up. The largest humming-
where a series of rapid strokes that bird is about 20 g, about the size of
causes the bird to rise is followed by a the average sparrow, but most hum-

78

1stPages_A.indd 78 7/22/20 10:48 AM

 mers average 3 to 6 g in weight. The wingspan of 6 to 8 m. They were able
wing loading associated with weights to take flight because of the strong and
above even 10 g must severely strain continuous winds that occurred in South
the hummingbird lifestyle. Second, America before the Andes arose; once in
hummingbirds feed on high-energy the air, they soared like condors. Fossils
foods such as nectar and small insects. of Pelagornis sandersi, an albatross-like
Such foods provide energetic rewards to bird that had long, skinny wings 6 to 7
match the energetic costs of harvesting m across, suggest that this species was
them. Third, hummingbirds reduce a highly efficient dynamic soarer over
energetic costs at night by going into the windy oceans of the past. Among
torpor. This allows them to drop their the largest of nonsoaring fliers are the
body temperature and metabolic rate swans, which reduce flight costs by fly-
so that they do not burn themselves out ing in formation and following favorable
before morning arrives (see chapter 8). winds on long-distance trips. Certainly,
It has been suggested that humming- mechanical traits restrain powered fliers
birds are no smaller than 2 g because from being much larger than any of the
the energetic costs of homeothermy are above, while energetic constraints result
too high to maintain body temperature in most flying birds being relatively
given the surface-to-volume ratio, and small.
also because bees and other insects with
low metabolic rates can more effectively Flightlessness
gather nectar at most small flowers.
When discussing wing loading, we Given the extreme energetic costs of
pointed out how bird weight increases flying, it is not surprising that when
faster than wing surface to the point birds find themselves in situations
that a limit to the size of the flying bird where they do not use flight, they lose
occurs. A larger bird needs larger wings, this ability. Since flight is critical to most
but to move these wings requires larger species for seasonal movements, finding
muscles, which at some point weigh food, and avoiding predators, it is also
too much for the bird to be able to fly. not surprising that most flightless birds
Where this limit to bird size occurs are relatively sedentary species that feed
in nature is unclear because larger on the ground or in the water and are
birds have developed methods to use either free of predators or able to elude
wind currents to increase lift without predators. It is also not surprising that
increases in size and power. Thus, the largest of birds, both modern and
condors, pelicans, and storks, which prehistoric, are or were flightless.
are among our heaviest fliers, have very Two modern groups of birds are
well-developed soaring abilities. totally flightless, the penguins and a
Fossil evidence suggests that even group called the ratites, which includes
larger flying birds once existed, with the ostrich. Penguins, of course, are
examples of both static and dynamic highly adapted to an existence in water,
soaring.5 The now-extinct family Tera- with heavy bodies and wings modified as
tornithidae contained condor-like birds paddles. They apparently evolved flight-
Flight

that weighed up to 80 kg and had a lessness early in their history, probably

79

1stPages_A.indd 79 7/22/20 10:48 AM

 as a result of several factors. We have groups are flightless. These include a
already seen how difficult flight is for flightless cormorant in the Galapagos
birds that are modified to be excellent Islands, a flightless grebe on Lake Titi-
divers. As the diving traits of reduced caca, flightless ducks in southern South
buoyancy and stronger legs developed in America and New Zealand, flightless
the evolution of penguins, the costs of pigeons in the southwest Pacific and
flying must eventually have become too Indian Oceans, a flightless parrot in
high, particularly for such large birds. New Zealand, and numerous flight-
Compensating for the loss of flight is the less rails. The Stephens Island Wren
fact that the highly modified penguin (Traversia lyalli; Acanthisittidae) of New
can avoid predators or migrate nearly as Zealand was the only known flightless
well in the water as it could by flying. It passerine.6 Not surprisingly, it went
is interesting to note that the ecological extinct when a cat was introduced to its
equivalents of penguins in north-tem- limited island habitat. Many of these
perate waters are generally smaller than flightless forms occur on islands, and
penguins. All of these use their wings many have gone extinct in recent times
as flippers when swimming and can fly, or are threatened with extinction by the
except the largest, the extinct Great Auk effects of introduced predators such as
(Pinguinus impennis), which was flight- cats and rats.
less and extremely penguin-like. Some exciting recent work on the
The ratites are a group of flight- paleornithology of Hawaii and other
less birds that includes the ostriches of islands has greatly expanded our knowl-
Africa, rheas of South America, emus edge of the occurrence of flightless
of Australia, kiwis of New Zealand, and island forms and the frequency and
cassowaries of New Guinea. These are causes of their extinction.7 One of the
nearly all very large, open-country birds most interesting findings of these stud-
that graze and eat some animal food ies is that flightless island forms were
such as insects. Though too large to fly, much more common in relatively recent
they can avoid predation by running very times than we had previously thought.
fast or delivering powerful kicks with Apparently, many of these forms were
their often-massive legs. These are birds very successful until primitive humans
of tropical grasslands whose movements arrived on the scene. Because humans
are generally limited. The kiwi is excep- are such efficient predators, at least
tional in being fairly small and noctur- 17 species of flightless birds from the
nal and having a diet of earthworms Hawaiian Islands have become extinct
within the forests of New Zealand. since the colonization of those islands
Evidence suggests that the ancestors by Polynesians about 1,500 years ago.
of both the penguins and the ratites Among these are flightless geese, ducks,
could fly. All have at least vestigial flight rails, and ibises.
quills and a cerebellum as in flying An equally impressive story is the
birds. Some show a pygostyle or alula, recent extinction of the flightless moas
chapter 3

structures unneeded if flight never of New Zealand.8 This group of at least

occurred. 13 and perhaps as many as 27 species
Single species of many other bird was last recorded alive in the late 1700s.

80

1stPages_A.indd 80 7/22/20 10:48 AM

 They were apparently thriving when size of a horse’s and a large, powerful
New Zealand was colonized by Maori beak (fig. 3.11).11 Diatryma or its relatives
natives about 1,000 years ago. The pre- appeared 60–70 million years ago and
vious success and diversity of the moas were probably replaced 10–20 million
in New Zealand was apparently possible years later by the development of modern
because these islands had never received mammalian carnivores, except in South
mammalian grazers or predators from America. This continent was isolated
nearby Australia. The moas became from the main flow of mammalian evolu-
the dominant grazers, occurring in a tion until about 4 million years ago, when
variety of sizes, including some larger it made a physical connection with North
than modern ratites. Although it appears America. During this period of isolation,
that the largest of these had gone extinct the dominant carnivores in South Amer-
before the arrival of humans, the latter ica were a group of birds known as the
event led to the eventual end of all these phorusrhacids.12 These were similar to
unusual birds. There were legends from Diatryma but apparently quicker runners.
the natives of New Zealand of a bird Phorusrhacids apparently became extinct
large enough to eat people, and recent quite rapidly when modern mammals
fossil evidence suggests this was in fact entered South America.
true, which is not too surprising given Other fossil discoveries indicate that
the lack of mammalian predators on that flightlessness has occurred in nearly
island. A recent set of fossils suggests all avian groups. For example, the West
that there was a giant flesh-eating stork Indies has had flightless hawks, vul-
on the Indonesian island of Flores, an tures, and owls, including a meter-tall
island also famous for its meter-tall owl that lived until the extinction of
“hobbit” people (Homo floresiensis). ground sloths and other mammals on
Whether these people were prey of the which it fed. Despite their diverse ori-
9
giant stork remains to be proved. gins, flightless birds share a number of
A similar story applies to the largest modifications. Among the first modifi-
of known recent birds, the Elephant Bird cations to occur with the loss or reduc-
(Aepyornis maximus) of Madagascar.10 tion of the role of flight is a reduction
This giant grazer and seed eater stood in the size of the wings and the flight
3–4 m tall and must have weighed nearly muscles of the breast. As we pointed out
500 kg. Its eggs were as large as 7 ostrich earlier, these muscles are very large, so
eggs or 183 hen eggs and served as excel- this reduction or loss results in a tre-
lent canteens for local residents until the mendous energy savings. A number of
bird became extinct in the mid-1600s. present-day species that can barely fly
The older fossil record shows some also show a reduction in breast muscles.
interesting flightless forms. Early in With time, modifications of the bone
the evolution of birds and mammals structure occur, particularly a reduction
and shortly following the extinction of in the size of the sternum (which is no
the carnivorous dinosaurs, many large longer needed for muscle attachment)
avian predators filled the carnivore role. and the pectoral girdle. Many of these
Among these was Diatryma, a massive changes may have occurred through an
Flight

predator about 2 m tall with a head the evolutionary process known as neoteny,

81

1stPages_A.indd 81 7/22/20 10:48 AM

 which refers to the maintenance of Fig. 3.11. A selection of flightless birds and
juvenile traits in adults. The young of how they compare to a typical human in size.
many birds have reduced breast muscles From the left we have an ostrich (Struthio),
and a small sternum until fairly late a predatory Diatryma, a kiwi (Apteryx), an
in their growth. Apparently, in some Elephant Bird (Aepyornis maximus), and a
species these morphological traits of phorusrhacid.
young birds have been maintained into
adulthood, resulting in flightless species.
Neoteny seems to occur regularly in the ing relationships. For example, scientists
rails, which have many flightless island who feel that all the ratite species are
forms. In contrast, the pectoral mus- related may have been misled by the
cles and sternum of chicken-like birds tendency of large, flightless, grazing and
develop fairly early in life, and this group seed-eating birds tend to end up looking
has never shown flightlessness. much alike. There are great similarities
The convergence in structure among between the leg of the flightless ibis once
flightless forms has caused a variety of found in Hawaii and that of the kiwi of
problems for people studying the pat- New Zealand, although these species
terns of relatedness among birds. These are very different in most other ways.
systematists (see chapter 6) often try to Despite these problems, unraveling
understand avian evolutionary patterns the mystery of the relationships among
by looking for similarities in such basic giant, nonflying birds continues to be
traits as the skeleton and muscles. When of great interest to ornithologists. The
birds with very different original shapes regularity of flightless forms shows the
chapter 3

share certain modifications after becom- extreme costliness of flight to birds, for if
ing flightless, major traits of bone and flight is not necessary, birds will quickly
muscle may be of little use in determin- adopt other means of locomotion.

82

1stPages_A.indd 82 7/22/20 10:48 AM

 C HAP T E R 4

Speciation
and Radiation

A
lthough the previous chapters lation is termed its fitness—the most fit
have attempted to define a animal is the one that most affects the
general model for a bird, it is genotypic characteristics of subsequent
necessary to mention some of generations. Generally, the animal with
the variations on this model. You need the set of genes best adapted to a set of
not take an ornithology course to know conditions should produce more young
that pigeons are different from sparrows than an animal with a set of genes more
and that many avian types occur. In this poorly adapted to these conditions. The
chapter, we will introduce you to how young of this favored set of genes should
this variety of birds has arisen. also produce relatively more young;
when this increased production of
Species and Speciation young changes the frequency of genes in
Natural selection the population, evolution has occurred.
For natural selection to drive the
All the adaptations that we will see in evolutionary process, the populations
this text, be they morphological, physi- on which natural selection works must
ological, or behavioral, are the result of provide some variability in genetic traits.
evolution. To understand these adapta- By choosing a subset of individuals from
tions, we need a fundamental knowl- this set of options, natural selection
edge of how natural selection works to can cause changes in gene frequency.
cause evolution. Without genetic variation, though, this
Natural selection can be most sim- process would not work. Thus, we see
ply defined as the differential perpetu- that populations that do not seem to be
ation of genotypes. Genotype, in turn, evolving still maintain a certain amount
refers to the genetic characteristics of genetic variability. Although this vari-
carried by an animal. For evolution to ability may seem costly because genetic
occur, natural selection must cause a recombination can result in geneti-
change in the genotypic composition cally unusual young that are selected
of a group of interbreeding animals against (a process known as stabilizing
(called a population). This change can selection), this variability also serves as
occur only through reproduction and an insurance policy for changing envi-
the differential survival and subsequent ronmental conditions, when genetic
reproduction of young. An animal’s abil- combinations that are not favored at
ity to add genetic material to the popu- present might become favored. With

83

1stPages_A.indd 83 7/22/20 10:48 AM

 these changing conditions may come for very red shoulders. At some point,
changes in gene frequencies and associ- though, these shoulders might become
ated changes in morphology or behavior: as red as they could get, which would
evolution. Such changes in the general stop the continued evolution of this trait,
genetic characteristics of a population or the cost of having redder shoulders
because of changing selection pres- that attract predators might not balance
sures are generally known as directional the reproductive rewards of this more
selection, because the genetic changes extreme color. At this point, stabiliz-
are usually related to changes in a char- ing selection would take over, and the
acter (such as size) in some direction. amount of red in the shoulder would not
Directional selection generally results in change over time.
changes in the average characteristics of Although models like the above are
populations, whereas stabilizing selec- easy to construct to explain the evolution
tion favors maintenance of average char- of a particular trait in birds, we must
acteristics with some variability around remember that since evolution often
this average. works through changes in gene frequen-
The evolution of every bird has cies in large populations, it is generally
involved numerous changes arising slow. Also, natural selection operates on
from directional selection, often with phenotypic characteristics, the expressed
periods of stabilizing selection occurring traits of genes; the difference between
between these periods of change. In genotype and phenotype slows down
many cases, a change in genetic traits the evolutionary process. The fact that
may lead to rapid directional selection most traits are determined by several
until those genes dominate the popula- genes and sexual recombination keeps
tion, at which point stabilizing selection mixing these genes together also slows
may take over until some new break- down evolution. While such a system
through occurs (either genetically or may seem wasteful and inefficient, this
environmentally). For example, we know conservative maintenance of variation
that male Red-winged Blackbirds (Age- allows populations to adapt to changing
laius phoeniceus) fight for breeding space conditions over long periods. A system
using red shoulders as an important part that allowed populations to quickly adapt
of their displays. We can envision that to short-term changes might not main-
the first male that evolved some red in tain enough variability for these popula-
the wing (perhaps through a mutation) tions to survive should further changes
may have had great success in intimidat- occur.
ing other males and attracting females
to breed. The offspring of this male that The species
inherited their father’s red shoulders
would have had similar success, until Natural selection acts on individuals, but
the population, through directional it is only by looking at the whole inter-
selection, was composed completely of breeding set of organisms (a population)
chapter 4

red-shouldered males. If the amount of that we can see how gene frequencies
red in the shoulder was important, evo- are changing and evolution is occurring.
lution would favor directional selection A closely allied but somewhat different

84

1stPages_A.indd 84 7/22/20 10:48 AM

 unit, the species, is the basic building concept defined above seems simple
block of avian taxonomy and the unit enough, applying it to real-world situa-
we will most regularly discuss in this tions leaves much room for controversy.
book. Although the species is such a For example, to determine whether
critical unit, there has been much recent we have a set of populations or a set of
controversy about the definition of this species involves seeing whether mem-
term, particularly a definition that covers bers of the different groups interbreed.
all species of plants and animals. As we Yet how do we do this in nature? Natural
examine the species concept and spe- conditions are critical, for some differ-
ciation in birds, keep in mind that such ent species are physiologically able to
controversy exists and may change our interbreed in captivity but never do so
ideas in the future. in the wild for behavioral or ecologi-
In its simplest form, a species can cal reasons. These various factors that
be defined as a group of interbreeding restrict the interbreeding of different
natural populations that is reproduc- species are termed reproductive isolat-
tively isolated from other such groups. ing mechanisms. Thus, different species
Thus, a species includes all the organ- must be reproductively isolated from
isms on earth that could be expected one another. Differences in plumage or
to exchange genetic material through behavior may be clues to reproductive
reproduction under natural conditions. isolation, but in some cases species of
In the case where a species is uniformly birds that look quite different will inter-
distributed over a relatively compact breed, while other populations that may
area, it may consist of only one popula- live together and look the same to us
tion. In cases where a species is found never interbreed.
in isolated patches of habitat (such as Although we will discuss taxonomy
a set of islands), each patch may have a in more detail later, we should review
population and relatively little exchange the nomenclature behind the species
of genes (termed gene flow) may occur concept. In addition to a common name
between populations. Yet if reproduc- (American Robin, Eastern Meadow-
tion can occur naturally under wild lark, etc.), scientists give each species a
conditions between members of these binomial scientific name that has Latin
different populations, they are still the or Greek derivations. The first part of
same species, unless their offspring are this binomial, the genus or generic
of demonstrably lower viability than name, may be applied to a set of very
normal. On the other hand, reproduc- closely related species and is used to
tion between members of two popu- designate close similarity. Since there
Speciation and Radiation

lations does not ensure that they are is no field test for congeneric species
of the same species. Distantly related (species of the same genus), this cat-
species occasionally hybridize; as long egory is a conceptual one and much
as these hybrids are of low frequency, argument occurs over which species
such hybridization does not negate the belong in which genus. The generic
species distinction, even if the hybrids name is followed by a species or spe-
are healthy. cific name that identifies that particular
Although the biological species species. Thus, the American Crow is

85

1stPages_A.indd 85 7/22/20 10:48 AM

 called Corvus brachyrhynchos. (Scientific uals in cages would not be of much
names are usually written in italics.) The value, as many species can interbreed if
genus Corvus includes all the large black confined in some fashion, even though
crows and ravens, while brachyrhynchos they do not do so in nature. Until recent
distinguishes this species from C. corax, advances in genetics, taxonomists were
C. ossifragus, and so on. Corvus is the forced to make fairly subjective judg-
Latin word for “raven,” and brachyrhyn- ments about such situations, some of
chos is Greek for “short-billed,” which which are still controversial to this day.
describes a crow compared to a raven. If Another problem with testing the
you understand a little Greek or Latin, biological species concept in nature
scientific names are sometimes helpful involves two populations that might
in describing bird characteristics, as in be separate species but do come into
the Northern Mockingbird (Mimus poly- contact and do interbreed and produce
glottos), Yellow-headed Blackbird (Xan- hybrid offspring. If some hybridization
thocephalus xanthocephalus), and House is allowed between what are still con-
Sparrow (Passer domesticus). When birds sidered separate species, when do we
are named after people, the scientific decide that too much hybridization has
name is not very descriptive. In other occurred?
cases, these binomials can be confusing. Some scientists question the useful-
Consider that the Puerto Rican Tody, a ness of any concept that cannot be tested
small fly-catching bird confined to that in the field; they feel a more realistic defi-
island, is named Todus mexicanus. Of nition of a species must be developed. In
course, if you do not understand much chapter 6 we will look further into the
Greek or Latin, the names are of limited methods of taxonomy and systematics,
use. In that situation, you can only won- with emphasis on modern techniques
der how Dolichonyx oryzivorus describes involving molecular genetics. For now,
a Bobolink (where Dolichonyx means it is important to know that to try to
“long-clawed” and oryzivorus refers to control such controversy and to ensure
eating lots of rice, which this species a consistent taxonomic system, com-
does on its wintering grounds). mittees of scientists rule on matters of
Despite its simplicity, numerous species designations. In North and South
problems exist with the biological America, final decisions on taxonomic
species concept. The biggest problems designations are made by a committee
occur with what we call allopatric popu- of the American Ornithological Society.
lations, which are populations that live Taxonomists involved in these decisions
in separate locations such that no inter- are often put into one of two categories,
action between populations occurs. For “lumpers” or “splitters.” Lumpers tend
example, an island system might have to put all closely related populations into
a bird that lives on several islands and a single species or similar species into
looks much the same on each. If there is the same genus. Splitters tend to focus
no movement between islands, we can on the differences between populations;
chapter 4

only guess whether the species would they are more likely to give separate pop-
interbreed if given the chance. Doing ulations specific status or place different
some sort of experiment with individ- species in separate ­genera.

86

1stPages_A.indd 86 7/22/20 10:48 AM

 In recent years, there has been Although most subspecies occur
much shifting of taxonomic designa- because barriers to gene flow result
tions among the world’s birds. Much of in isolated populations, this is not a
this reflects an accumulation of informa- requirement. Species with broad ranges
tion from modern studies of DNA and but little mixing of the population may
DNA sequences. As we will see, even the show gradual changes across their
quantification of vast amounts of genetic ranges. Thus, even with a continuous
data does not answer all questions. As distribution of a species across an envi-
long as taxonomic decisions must be ronmental gradient, species members at
based on human judgment to some one end of the range may look different
extent, there will be controversy and a from members at the other end. This is
continued place in ornithology for avian termed a cline, or clinal variation, and
systematists and taxonomists. results from the combined effects of
different natural selection pressures in
Variation within species different parts of a species’ range and
slow gene flow within the species, such
So far, we have examined the popula- that regionally adaptive traits are not
tion—the interbreeding set of organ- swamped by interbreeding with individ-
isms that serves as the basic unit of uals from other areas.
evolution—and the species—the total Among the factors that may accen-
of all potentially interbreeding popula- tuate or retard subspeciation in birds
tions. Consider a species with a broad are migratory behavior, homing abil-
geographic range. If this range is broken ity, mate selection behavior, and song
into separate sections by a barrier such dialects. Nearly all species of birds have
as a mountain range or ocean, each been divided into subspecies based on
section will most likely contain a pop- differences in plumage, song, and other
ulation where more reproduction will traits. For example, the White-breasted
occur between members of that pop- Nuthatch (Sitta carolinensis) has been
ulation than with members of distant divided into multiple subspecies, all
populations. Thus, gene flow between of which have slight plumage differ-
populations will be restricted. Next, ences and occupy a different part of the
imagine that each population lives in nuthatch range; some have suggested
slightly different conditions such that that this could really be three species.
the most adaptive plumage in each Note in figure 4.1 that the nuthatch
region is slightly different. If there is not has a broad range across most of North
too much exchange of genes between America (the green area); this range
Speciation and Radiation

populations, we could get populations includes all areas where nuthatches are
that differ in plumage. In most cases, seen with some regularity. But it also
these populations are termed subspecies shows where nuthatches are during the
or geographic races. As long as these breeding season, as indicated by the
populations can interbreed or potentially North American Breeding Bird Survey.
interbreed, they are still considered one These breeding areas can be divided
species, even though they may show into three major areas (with multiple
distinct differences. colors), which suggests some allopatry

87

1stPages_A.indd 87 7/22/20 10:48 AM

 during the breeding season, a situation the subspecies occurs, as in the prairie
that may disrupt gene flow. Note that subspecies of the Canada Goose (Branta
the three populations of nuthatches also canadensis interior). In other cases, it
look slightly different, which has led to may distinguish a morphological trait
the suggestion that they may really be of the subspecies, as in the giant race
three species. of Canada Goose (Branta canadensis
Three subspecies is a relatively low maxima). A species with no described
number; the Song Sparrow (Melospiza subspecies is given only a binomial.
melodia) is often considered the classic Because the act of distinguishing
example of subspeciation, with 30 or full species of birds can be somewhat
more races that vary in size and plum- arbitrary, many people feel that trying
age in response to the variety of eco- to name and distinguish subspecies
logical conditions in which this species is so arbitrary as to be a waste of time
lives. A large geographical range does (see Suggested Readings). The Amer-
not guarantee subspeciation. In the ican Ornithological Society Check-list
Northern Pintail (Anas acuta), pair for- Committee has not updated subspe-
mation occurs on the wintering grounds cific designations for North American
where birds from all of this species’ birds for several decades. On the other
breeding range congregate. hand, detailed examinations of different
Females return to the general area subspecies of birds often lead to studies
where they were hatched, and their that support the splitting of these pop-
mates follow. As a result, there is exten- ulations into separate species, as might
sive gene flow and no subspeciation. occur for the different populations of
In contrast, populations of the Canada nuthatches shown in figure 4.1 and as
Goose (Branta canadensis) are very social occurred for the geese shown in figure
throughout the year. Because they tend 4.2. Although nearly everyone now
to winter and breed together in tradi- agrees that trying to put distinct names
tional locations and mate for life, gene on gradually changing populations is
flow between populations is reduced. fraught with difficulties, many feel that
For a long time, this was considered it is important to recognize and cate-
one species with as many as 17 races, gorize in some way the great variability
although recently one author suggested that can occur within a species to truly
this species had 218 races.1 Currently, understand the dynamics of the avian
this species is split into two groups, the speciation process.
small Cackling Goose (Branta hutchin-
sii, with five subspecies) and the larger The dynamics of reproductive isolation
Canada Goose (B. canadensis, with seven
subspecies; fig. 4.2). So far, we have seen how the restric-
Scientific nomenclature for sub- tion of gene flow between populations
species uses a Greek or Latin trinomial. can lead to variation between these
In addition to the genus and species populations in morphological or behav-
chapter 4

name, a subspecies name is added. In ioral traits. What happens if the gene
some cases the subspecies designation flow between two populations is very
refers to the geographic location where restricted and changes occur in repro-

88

1stPages_A.indd 88 7/22/20 10:48 AM

 Fig. 4.1. Distribution of the White-breasted are recorded in surveys during the breeding
Nuthatch (Sitta carolinensis) across North season. Note that this results in three separate
America and how that may affect taxonomic populations with subtle differences in plumage,
decisions. The colored areas on the map show which may or may not interbreed and which
the total range of this species; the areas with may be split into three separate species.
colors other than green show where nuthatches

1stPages_A.indd 89 7/22/20 10:49 AM

 Fig. 4.2. Three subspecies of Canada Goose Deciding when two populations are in
(left) and one subspecies of the Cackling Goose fact reproductively isolated is the prob-
(right), all of which were once considered the lem, as mentioned earlier.
same species. To understand how speciation has
occurred in nature, we need to examine
ductive behavior? Quite simply, if the the ways that natural conditions can pro-
two populations change so that they no duce allopatric populations. Generally,
longer interbreed under natural con- geographical or ecological barriers to a
ditions, they will be considered repro- population’s distribution are involved.
ductively isolated and, thus, separate A lowland bird found on both sides of a
species. mountain range could undergo spe-
The simple models for avian spe- ciation. Colonization of a set of islands
ciation work much the same way as the could result in a species on each island.
situation above. They generally require Long-term changes in geography such
that populations become allopatric (sep- as continental drift could isolate popu-
arated geographically) such that gene lations, as could climatic events such as
flow between them is disrupted. With glaciers.
time, changes should occur in repro- We will examine some of these
ductive behavior such that members of mechanisms in more detail later. Mean-
chapter 4

the two populations will not interbreed. while, having looked at reproductive
This is the reproductive isolation that is isolation, we should be aware that it is
required by our definition of a species. only one of the critical mechanisms that

90

1stPages_A.indd 90 7/22/20 10:49 AM

 produce avian diversity. Imagine a world have some slight advantage and will
with only one species of parrot. Assume eventually competitively exclude the
this parrot eats the same type of food other. Because this principle was derived
in all the parrot habitats of the world. from the work of G. F. Gause (1934), it
Because this species is found on sepa- is sometimes called Gause’s principle.
rate continents, or in forests separated The total of an organism’s properties can
by mountains or deserts, populations of be called its ecological niche, and the
the parrot may become reproductively principle can be restated as “two species
isolated. A good parrot taxonomist with identical niches cannot coexist.”
might recognize a number of parrot For the competitive exclusion
species, but only one species would exist principle to function, the two coexisting
in each patch of parrot habitat. To under- species must periodically be put in a
stand fully how avian speciation may situation where resources are limited
lead to increased avian diversity, we need enough that competition for them
to know how one parrot species can occurs. If resources were superabun-
become two or more species that live dant, we could visualize two species with
together in a single forest. To do this, identical ecologies coexisting for some
we must add ecological factors to the time, but no system could maintain this
reproductive factors we have analyzed superabundance of resources indefi-
thus far. nitely. We would expect that the species
using these resources would increase
Competitive Exclusion in density until the resources finally
and Ecological Isolation became limiting. At this point, compe-
tition would ensue and the competitive
Two species derived from a single paren- exclusion principle would become oper-
tal species (such as the parrots above) ational, to the detriment of at least one
once shared not only reproductive traits, of the species.
but ecological traits. Should both pop- As an ecological theory, the compet-
ulations expand their ranges following itive exclusion principle suffers from
reproductive isolation, these two spe- several problems. While it is easy to
cies may attempt to live in sympatry approach with simple mathematical
(the same geographic area). Because models or laboratory experiments, it is
of their identical ecological histories, difficult to test in the field. With all the
when they attempt to coexist they may various parameters involved, we cannot
interact when foraging to a great degree. measure “identical ecologies.” Moreover,
Whether they will be able to coexist if the principle really holds, we should
Speciation and Radiation

successfully depends on a basic tenet never expect to find coexisting species

of ecology, the competitive exclusion with identical ecologies unless the two
principle. species have only recently come into
The competitive exclusion principle contact. When two identical species
states that two species with identical attempt to coexist over time, one will
ecological traits cannot live in the same either exclude the other or evolve differ-
place at the same time. Should they ences that allow the species to coexist.
attempt to do so, one of them should Thus, in nearly all cases, we see only

91

1stPages_A.indd 91 7/22/20 10:49 AM

 the aftereffects of competition (which Isolation by differences in range
some call “the ghost of competition
past”). This is support for the model, but Related species that are isolated by
in a roundabout way. Because of these differences in range are ecologically
problems, most ecologists have worked very similar but not sympatric. Rather,
with corollaries of the competitive exclu- these species live in different locations
sion principle. For example, if species (allopatry); their ecological isolation
with identical ecological traits or niches mechanisms can be shown on a map.
cannot coexist, we can hypothesize that Should the nuthatches in figure 4.1
coexisting species must differ to some be split into three species because it is
extent in the totality of their ecological decided that the populations are repro-
traits. We can then ask questions about ductively isolated from one another, we
how similar coexisting species can be would not expect them to spread and
and the ways in which species separate overlap in their breeding range. Across
the environment to allow coexistence. the world we can find overlapping
The ways in which coexisting species of nuthatches, but these coexist-
species separate ecologically are often ing species are always of very different
termed ecological isolating mechanisms. sizes (see below). Since there are other
Books that survey these mechanisms species of nuthatches that are half as big
suggest the following general categories: as the White-breasted Nuthatch shown
(1) isolation by differences in range, (2) in the figure, we would probably never
isolation by habitat, and (3) separation by see these separate populations of large
differences in food or foraging behavior.2 nuthatches expand and overlap. But if
Let us examine each of these categories they are deemed to be good species, this
in turn. As we begin, we must remind is a great example of how the diversity of
ourselves that species that are closely North America is enhanced by similar
related by history are also usually very species that coexist by differences in
similar in morphology and behavior, range across a broad geographic area.
which means that they likely use the The recent reorganization of the
same foods in similar ways. Thus, birds Rosy Finches (Leucosticte) may serve as
of the same genus or family are more another excellent example of separation
likely to interact with one another than by range, as the three species of alpine
with those of different genera or fam- tundra finches have nonoverlapping
ilies. The strongest such interactions breeding ranges in North America.
may occur when populations of the Originally, there was just one species
same species spread across a region and of Rosy Finch (L. arctoa) with three
become separate populations. Here we subspecies, which are now species.
have species that started out with the The type of distribution they evince is
same ecological requirements, which called a displacement pattern to distin-
means that should they attempt to inter- guish it from other forms of ecological
act, competitive exclusion might be very isolation, for in this situation, the birds
chapter 4

strong because of their original strong have not evolved mechanisms to truly
similarities. coexist. Rather, when we look at the
whole of North American alpine tundra

92

1stPages_A.indd 92 7/22/20 10:49 AM

 as a resource, we see that these species, species never actually coexist because of
which undoubtedly share a common their habitat separation. A good example
ancestor, have ensured their existence of this occurs among the Empidonax
on the continent by dividing the moun- flycatchers of eastern North America.
tain resources geographically. Although remarkably similar in size and
plumage, each Empidonax species has a
Isolation by habitat habitat distinct from that of the others.
Although different species may live next
Birds that separate by habitat may have to one another, their territories never
the same ecological traits in the same overlap. Very subtle habitat differences
general area, but a closer look reveals may be used for separation between spe-
that they occupy different specific areas. cies using this mechanism, especially in
They may have overlapping ranges as the tropics. In contrast, some grassland
shown on a map, but they are not all in birds separate by habitat according to
the same place at the same time. There vegetation density and height, factors
are several ways to do this. that also might be modified by cattle
Segregation by altitude. Going up a grazing.4
mountain slope, we may find closely Within-habitat isolation. Many species
related species replacing one another at are able to achieve ecological isolation
various elevations. In some cases, this even when they are syntopic (living in
appears to be a geographic replacement the same location). These species may
related to interactions between species, overlap in the areas where they feed
while in others it may be related to hab- such that a census of birds taken at one
itat changes. During an extensive study point would end up counting them all,
on Andean bird distributions,3 research- but closer examination will reveal that
ers found that about one-third of the they are using either different foods
species recorded were part of altitudinal or different foraging techniques (see
replacement series. As they went up the below) or subdividing the habitat in
mountain, when the range of a conge- some way.
neric species of a particular size ended, The classic study of habitat subdi-
an ecologically similar relative replaced vision to achieve ecological isolation
it, filling the same ecological niche. As was done by Robert MacArthur (1958).
many as four species of related, eco- In the years following the formulation
logically identical birds were observed of the competitive exclusion principle,
subdividing a mountain in this way, some ecologists pointed out sets of birds
with many different types of birds using they felt disproved the principle. Among
Speciation and Radiation

this mechanism of coexistence along the these examples were five species of
mountain slope. Setophaga (formerly Dendroica) warblers
Between-habitat segregation over small that have similar morphologies, behav-
distances. Birds with essentially identi- iors, and food habits and all live together
cal ecologies may be found in the same in spruce forests in New England. By
geographic region but be ecologically looking closely at the foraging behavior
isolated by habitat type. Although the of these species, MacArthur showed that
ranges of these species overlap, the each had a zone within the spruce tree

93

1stPages_A.indd 93 7/22/20 10:49 AM

 Fig. 4.3. Habitat separation by five coexisting ics, some species do all their foraging
warblers in a spruce forest, showing how they in bromeliads, while others search for
all live in the same general area but specialize food only in dead leaves still hanging
on specific portions of a spruce tree. on a branch. Some of these species also
have specialized foraging behaviors and
should be included in the next section,
where it did the majority of its foraging but in the sense that they have chosen
(fig. 4.3). Each species spent its time in a part of the habitat in which to isolate
a different zone, thereby maintaining themselves ecologically, they are similar
ecological isolation. to the species that use vertical habitat
In deciduous or tropical forests with separation.
more uniform vegetation from the forest
floor to the canopy, closely related birds Separation by differences
often separate by the mean foraging in foods or foraging behavior
height they use. An excellent example
of this occurs with the antwrens (Myr- So far, we have examined methods by
motherula) of Peru.5 Each of these nearly which birds with similar ecological
identical species has a zone above the traits partition where they live. Now let
forest floor where it forages that dif- us examine ways in which species that
fers in large part from the zones used live together and have similar ecologies
by other Myrmotherula species. Other separate by the foods on which they live
examples of such habitat subdivision by or the ways they capture this food.
layering exist, particularly in species-rich Food type and size. The simplest type
tropical forests. In some cases, the birds of ecological isolation by food occurs
using the same layer stay together in when two species have totally different
large foraging flocks (see chapter 7). food habits. A bird that eats fruit has few
In other cases, coexisting species problems coexisting with a bird that eats
chapter 4

may specialize on particular types of insects. Usually, birds taking such dif-
vegetation within a forest, such as vine ferent resources are of different enough
tangles or shrubby growth. In the trop- morphology (especially bill size and

94

1stPages_A.indd 94 7/22/20 10:49 AM

 structure) that their ecological interac- by size are fairly common in nature.
tions are not pronounced. They are also An increase in size of 1.2–1.4 times the
usually distantly related, which leads to smaller species in length or 2 times
the general observation that taxonom- in weight is commonly seen in these
ical differences are also related to the series, although why these factors are
strength of competition between spe- so prevalent is a mystery.7 The Tufted
cies. When we look within sets of related Titmouse (Baeolophus bicolor) and
and coexisting seed eaters or fruit eaters either the Black-capped Chickadee
we expect important patterns of eco- (Poecile atricapillus) or its close relative
logical isolation, but when we compare the Carolina Chickadee (P. carolinen-
distantly related members of these sets sis) coexist in much of eastern North
we expect less strong interactions, with America; the titmouse weighs about
little competition between members of 22 g while the chickadees (which do not
the different sets. coexist; see below) weigh about 11 g. In
Differences in the size of the bill or tropical America, five species of king-
body are the main ways that competing fishers coexist and differ by approximate
birds separate within food types. Stud- doublings in weight (fig. 4.4). Other
ies have shown that bill dimensions are examples of coexisting birds that differ
often related to the mean size or hard- by body size or bill size can be seen by
ness of food the bill can handle. Body paging through any bird book. While
size apparently affects the size of food a there has been much recent controversy
bird can most efficiently handle or the about the meaning of the frequently
size of food it must harvest to be ener- seen ratio of 1.3 in length or 2 in weight
getically efficient. Several studies have (termed the Hutchinsonian ratio after
shown the relationship between body or G. E. Hutchinson, who made it famous),
bill size and mean prey size.6 Because the important point is that differences
bill and body size often vary together,
it is sometimes difficult to separate the Fig. 4.4. Five coexisting kingfishers of the New
effects of each. World. All of these specialize on eating fish,
Series of coexisting congeners but each species specializes on a different size
(birds of the same genus) that separate of fish.
Speciation and Radiation

95

1stPages_A.indd 95 7/22/20 10:50 AM

 in body or bill size can ensure ecological (fig. 4.5);8 these movements are appar-
isolation. ently correlated with the way the birds
Foraging differences. Two species of search for insects and the types of prey
birds may be living together and eating they capture.
the same size of similar prey, but if they Time. Certain birds appear to sepa-
are capturing this prey in a different rate resources on a temporal, often
manner or different location they may nocturnal-diurnal, basis to allow their
be adequately separated. A simple exam- coexistence. Owls and hawks are good
ple of this is the difference between a examples of ecological equivalents that
10 g flycatcher and a coexisting 10 g war- coexist by dividing time. In a few cases,
bler. The insect sizes these birds eat may it appears that two similar species may
be similar, but the flycatcher catches its time their breeding seasons so they
prey on the wing (usually flying insects) do not overlap. The feeding of young
while the warbler eats insects and larvae requires enough extra food that two
picked up from branches. Some of the competitors with simultaneous breeding
same insects could be eaten by both, but seasons perhaps could not both breed
their differences in foraging technique
are apparently enough to allow their Fig. 4.5. Movement patterns of North
coexistence. Another study has shown American grassland birds that may explain
how sets of coexisting grassland birds how these species can coexist in a fairly simple
feed with different rates of movement habitat (Cody 1968).

96

1stPages_A.indd 96 7/22/20 10:50 AM

 successfully. By having separate breed- a species. Rather, we see the results of
ing times, both may be able to coexist. previous interactions. One of the best
ways to appreciate that competition is
Combinations of isolating mechanisms real is to look at how a single species
reacts to different competitive environ-
Although we have classified three ments. One way this can be done is to
distinct types of isolating mechanisms, look at a species in different parts of its
they can work in combination to ensure range where different competitors live.
the ecological separation of two spe- Islands are often excellent environments
cies. Thus, a little size difference and a for such comparisons because they are
little foraging height difference may be discrete units that often have relatively
enough to isolate two species. Groups low numbers of competitors such that
of congeners exist that use multiple the interactions between two species
techniques. John Terborgh had five are fairly visible. Based on his studies of
species of Basileuterus warblers on his the distributions of birds on Southwest
9
Andean study sites. These came in Pacific islands, Jared Diamond (1979)
two size classes. Members sharing the has described a number of changes
same size differed in elevational range, resulting from changing competitive
but members of the two sizes could pressures. Among the most common
coexist. Woodpeckers are another group niche shifts in the absence of competing
in which coexisting birds often differ species were expansions in the altitudi-
by size, while similar-sized woodpeck- nal range of a species, the types of habi-
ers specialize in different habitats in a tats it used, or the vertical zone within a
region. habitat where the species would forage
There has been much theoretical (fig. 4.6). Not surprisingly, species living
discussion about patterns in the amount in these situations often show increased
of total separation that is necessary for densities, as they are effectively able to
ecological isolation. Some evidence feed on most of the food that once sup-
suggests that tropical mainland birds ported two or more species. Diamond
can divide habitats and resources more found that shifts in diet or foraging tech-
finely than birds of the temperate zone. nique were rare, which is not surprising
While this may be true, it is also possi- since these shifts involve severe changes
ble that tropical birds may be separating in morphology, physiology, and/​or
in subtle ways that we do not yet under- behavior. Similar patterns of niche shifts
stand. As we will see later, attempting have been shown in other island sys-
to understand the ecological isolating tems and on what are effectively “moun-
Speciation and Radiation

mechanisms used by several hundred taintop” islands (see chapter 5).

coexisting species can be a challenge. Another type of niche shift that
has evoked much controversy involves
Support for competition theory a shift in bill or body size caused by
changing competition. Such a shift is
We mentioned earlier that competition often called character displacement
is a difficult phenomenon to understand because the change in competitive
because we rarely see it directly affecting pressure “displaces” a morphological

97

1stPages_A.indd 97 7/22/20 10:50 AM

 Fig. 4.6. Variation in elevational distribution pick insects from bark in East Asia
(top) and foraging height distribution was once considered the classic case
(bottom) with the number of coexisting of character displacement (fig. 4.7).
species, which is related to island size. With These species are of the same size
fewer competitors, a species can expand its when they live alone but diverge in
altitudinal range or the foraging height it can size where they coexist, an apparent
use (Diamond 1977).
case of competition-caused character
displacement. This example has been
character in some direction. Let us disputed, though, because the species
visualize two coexisting species that are show evidence of shifting size before
very similar in the foods they eat, except they come into contact.10 To some, this
that because they differ in body size, shift suggests that it is the traits of the
there is a difference in mean food size. environment of each nuthatch that are
If one of these species was absent, we changing and causing the niche shifts
might expect the other species to shift (and perhaps allowing the coexistence of
to a more intermediate size so that it the two species), rather than the interac-
could use a wider range of the available tions between the two species. Defend-
food (including that used by its former ers of character displacement argue that
competitor). Depending on which spe- such shifts simply reflect the fairly con-
cies was absent, this shift could involve servative nature of body size as a genetic
either an increase or decrease in size or trait, such that it is not surprising that
chapter 4

weight. gene flow causes some size shifts within

A situation involving nuthatches a population outside the actual zone
(Sitta neumayer and S. tephronota) that of contact between species. Obviously,

98

1stPages_A.indd 98 7/22/20 10:51 AM

 proper understanding of the role of reflects the difficulty of studying com-
competition here requires knowledge petition, while part of it reflects cases of
of all the foods available throughout sloppy science, where researchers have
the ranges of both species, how these too easily explained observed patterns
are subdivided both within the zone of with competition theory without con-
sympatry and outside it, and the genetics sidering other explanations. After a
of size determination and rates of gene rigorous examination of both competi-
flow. Several recent studies on size shifts tion theory and the support for it, there
have made convincing cases for charac- seems to be enough evidence that it
ter displacement as a viable mechanism plays a strong role in the evolution of
to reduce competition between species birds.11 There are just too many patterns
in certain situations (see chapter 5). in the abundance, distribution, and
There has been much criticism of behavior of birds that can be explained
competition theory in recent years, and only as adaptive responses to the peri-
some scientists feel the importance of odic scarcity of some resource. Although
competition in birds’ lives has been the previous material has focused on
overemphasized. Part of this controversy foods during the breeding season, com-
petition can also occur in other situa-
tions, such as on the wintering grounds,
Fig. 4.7. Character displacement in bill length
while migrating, or when searching
in two species of nuthatch that allows them to
coexist by being of different sizes (Brown and
for nesting sites. It is also apparent
Wilson 1956). that competition need not occur only

Speciation and Radiation

99

1stPages_A.indd 99 7/22/20 10:51 AM

 between similar species of birds; when- In some cases when populations
ever two organisms use similar foods make secondary contact, reproductive
there is the possibility for important isolation may not initially be complete,
competitive interactions. Thus, while but the differences between populations
some ecologists have attempted to prove result in hybrid offspring that are less
that competition between similar spe- viable than offspring of mating between
cies of birds has been overemphasized, parents of the same population. In this
others have pointed out strong competi- case the two species are considered valid
tive interactions between birds and spi- and the hybrids are “noise” in the sys-
ders, bats, monkeys, and other animals. tem. Because the production of hybrid
While such factors as predation, food young greatly lowers the fitness of the
supply, and environmental traits are birds producing the hybrids, we would
obviously of enough importance to birds expect natural selection to strengthen
that they must not be ignored, compet- the reproductive isolating mechanisms
itive interactions are a major force in of these two species.
determining the diverse characteristics When reproductive isolation
of the birds we see today. between two species is complete, the
result of secondary contact between two
Mechanisms of Speciation related species depends on ecological
considerations. If no ecological changes
Now that we have looked at the essen- have occurred in either population, the
tials of both reproductive isolation and two populations may expand only to the
ecological isolation, let us put them point of recontact and then stop because
together and examine the complete they competitively exclude one another.
speciation process. We start with two Species with ranges that come together
populations of the same species that but do not overlap are termed parapatric.
have been allopatric for some time. If The distribution of Rosy Finches that we
they expand their ranges and make con- looked at earlier probably arose in this
tact with one another, several things can manner; other examples follow.
happen. If the populations are not repro- When reproductive isolation is
ductively isolated, interbreeding may complete and the populations have even
occur and gene flow between the popu- slight ecological differences, some form
lations will begin. Depending on the rate of coexistence mechanism may evolve
of gene flow, any differences between to allow both species to expand to parts
the populations that may have evolved or all of the other species’ range. Often,
during allopatry may either disappear this process is characterized for a period
or remain with a zone of intergradation by a situation in which each species
of forms. If these differences include lives largely alone but there is a zone of
plumage differences, the zone of contact overlap. In this zone of sympatry, inter-
may be characterized by individuals with specific competition is accentuated, and
plumages intermediate between those character displacement or other ecologi-
chapter 4

of the two populations. In either of these cal shifts may take place. Through natu-
cases, speciation is not complete and we ral selection the two species may eventu-
still have just a single species. ally evolve sufficient ecological isolating

100

1stPages_A.indd 100 7/22/20 10:51 AM

 mechanisms for range-wide coexistence. be explained by looking at the effects
The extent to which their ranges finally of glacial movement during the past
overlap depends on a number of factors, 100,000 years or more, the Pleistocene.
many of them related to community During this period, advancing glaciers
structure considerations that we will pushed forest habitats far to the south
look at in chapter 5. It is important to and may have separated them because of
remember that only through the effects the arid grasslands that occurred in the
of both reproductive and ecological iso- southern Great Plains region. This could
lation can we go from one species to two have caused allopatric populations and
species in an area, but a gradient exists initiated the speciation process. With the
to the extent that either or both of these retreat of the glaciers and expansion of
processes occur following the separation forests, these populations would have
of populations. expanded and once again made contact
The above analysis essentially in the north (fig. 4.8).
develops a model for allopatric spe- Robert Mengel (1964) has presented
ciation that involves the disruption of the most intricate examination of this
gene flow through allopatry, divergent process with his analysis of the evolution
selection so that reproductive isolation of the New World wood warblers (family
evolves in the two populations, eco- Parulidae). His model shows how the
logical isolation either before or after expansions and contractions of glaciers
recontact of the populations, and finally, could have provided the conditions to
two sympatric species where formerly produce new species. He then compares
only one occurred. How might all these this model with the distributions and
steps occur in nature? Unfortunately, morphological characteristics of current
scientists have not been around long species to piece together how sets of
enough to observe the speciation pro- species (termed superspecies) arose.
cess (although it is possible that a new Much of his examination of interactions
species of finch on one of the Galapagos between potential species occurred in
Islands has been observed).12 Rather, a region of western Canada where the
they can try to fit the model described forests from the east and those from
above with present-day patterns of distri- the west came together as the glaciers
bution and historical patterns of climate, retreated toward Alaska. In this region
geology, and so forth. In many cases, about 6,500 years ago, populations that
much can be learned from studies on had been living in allopatry during a
populations that did not quite complete period of glacial advance came together.
the speciation process. Let us examine Here we can see how they interacted
Speciation and Radiation

some examples. and how speciation did or did not occur,

depending on the development of
Pleistocene glaciation and reproductive isolation, and whether or
speciation in North America not new species might have overlapped
because of the existence or development
Many of the most obvious examples of of ecological isolation.
recent speciation or subspeciation in Of course, modern distributions do
the North American avifauna can best not tell us everything, and not all the

101

1stPages_A.indd 101 7/22/20 10:51 AM

 Fig. 4.8. Habitat distribution of North America between these forms was regular and
today (left) and during a recent glacial event the young were viable, so now they are
(right). The Great Plains (brown) separates considered races of the Yellow-rumped
eastern and western forests in the United Warbler (Setophaga coronata). Many
States today, but these forests are connected in other species or subspecies appear to
Canada. During glacial advances, eastern and have originated through the effects of
western forests were very allopatric, which may isolation caused by glaciation. Until
have led to avian speciation. recently, ornithologists recognized three
species of flickers (Colaptes) in North
America. These “species” were thought
species involved were perfectly isolated. to have parapatric ranges with a narrow
There have undoubtedly been extinc- zone of hybridization where the popu-
tions of some populations; this may help lations made contact. Because birds of
explain imbalances between species different plumages regularly interbred
occurring in different areas. In certain where they overlapped and produced
cases of superspecies evolution, some of young with intermediate plumages, sug-
the derived species are unable to live in gesting that reproductive isolation had
sympatry. Hybrid zones or incomplete not occurred, these species were com-
speciation has occurred in other cases. bined into the Northern Flicker (Colaptes
The Myrtle Warbler and the Audubon’s auratus). More recently, though, sci-
chapter 4

Warbler were once considered distinct entists decided that the desert form
species that overlapped in a small area. of flicker was reproductively isolated
Studies showed that hybridization from the others, so it was restored as a

102

1stPages_A.indd 102 7/22/20 10:51 AM

 separate species, the Gilded Flicker (C. Where it occurs, this gap of up to 24 km
chrysoides). Because these species all are may reflect the results of low success
the same size, they fill the “flicker niche” of hybrid offspring and selection for
among woodpeckers and do not overlap reproductive isolation by avoidance of
in range. the potential hybrid zone. It is interest-
A somewhat different situation ing to note that the Carolina Chickadee
occurs in the meadowlark species that moves to higher elevations on moun-
most likely evolved following glacial tains where the Black-capped Chickadee
movement, but in a different way. As is absent, which is what we would expect
a grassland bird, the ancestor of these when competition is involved.
meadowlarks had allopatric popula- Not all species that had allopatric
tions among the separate grasslands populations during the ice ages were
that occurred when the glaciers moved able to expand their breeding range
southward, which allowed them to all the way to where the forests came
become separate species. Currently, the together as they followed the glacial
Eastern Meadowlark (Sturnella magna) retreat. Many forest or forest edge spe-
and Western Meadowlark (S. neglecta) cies were separated by the grasslands
have largely separate ranges but overlap of the Midwest and existed in allopatric
in a rather broad zone of the central populations for the long periods when
United States. In this zone they tend to glaciers were present. In these cases,
separate by habitat type, with the eastern the new species that frequented eastern
species preferring wetter sites and the and western forests but did not go as far
western species drier slopes. In addi- north as Canada never had a chance to
tion to these habitat differences, these interact because they were separated by
species have evolved decidedly different the vast grasslands of the Great Plains of
songs. Although hybrids do occur, they the central United States. But as Euro-
are very rare. pean Americans settled these plains over
The mechanisms of ecological the past 200 years or so, fires became
and reproductive isolation between less frequent and forests tended to
two species are not always consistent develop along the rivers that came out
throughout their zones of contact. The of the Rocky Mountains and flowed east.
Black-capped Chickadee and Carolina As these forests developed, birds from
Chickadee have essentially nonover- the east moved to the west, and those
lapping ranges in the eastern United from the west moved to the east. They
States (fig. 4.9). Along much of the met along the 100th meridian, where a
zone of contact the breeding ranges of great deal of interaction between poten-
Speciation and Radiation

these species are contiguous and occa- tial species was observed (table 4.1),
sional hybrids occur, but along parts much of which had existed for only a
of the zone in Illinois, Indiana, and hundred years or less.
Ohio, a gap in the range of the species A tremendous amount of activity
occurs.13 A similar gap occurs on some regarding species designations has
Appalachian mountains where these occurred in this region over the past
species separate by altitude, with the few decades. A great deal of lumping of
blackcap living above the Carolina. species occurred in the 1970s, including

103

1stPages_A.indd 103 7/22/20 10:51 AM

 Fig. 4.9. Range of the Black-capped Chickadee
and Carolina Chickadee, two species that may
be the result of allopatry during glacial periods,
but that cannot coexist and so separate by
range, with the Carolina confined to the
southeastern United States.

1stPages_A.indd 104 7/22/20 10:52 AM

 in such groups as the flickers (men- some of these species pairs resulted in
tioned earlier) and orioles. For example, support for splitting them again into
the Baltimore Oriole (Icterus galbula) and separate species, which occurred with
Bullock’s Oriole (I. bullocki) were fused the flickers, orioles, and towhees. A
into the Northern Oriole (I. galbula). For great deal of work has been done in this
a few species (towhees, grosbeaks, and region, but much remains to be done.
buntings), many hybrids in this region
were observed, but the eastern and west- Speciation patterns in tropical America
ern forms were not formally combined
into a single species. In the case of the In looking at the process of allopatric
Indigo Bunting (Passerina cyanea) and speciation, we have seen how geo-
Lazuli Bunting (P. amoena), researchers graphic barriers or extreme climatic
studying the interacting species sug- fluctuations such as glaciers can isolate
gested that the species were developing populations. Yet the Amazon basin of
different calls in the zone of overlap, South America has one of the most
so they were kept as separate species.14 diverse avifaunas on earth even though
A decade or so later, detailed studies of it has few geographic barriers and has

Table 4.1
Species that are known or suggested to hybridize within the Great Plains as wood-
ed habitats connected eastern and western populations of similar species
eastern form western form hybrids studied?
Eastern Screech-Owl Western Screech-Owl Rare No
Yellow-shafted Flicker Red-shafted Flicker Common Yes
Red-bellied Woodpecker Golden-fronted Woodpecker Rare No
Great Crested Flycatcher Ash-throated Flycatcher Unknown No
Eastern Wood-Pewee Western Wood-Pewee Unknown No
Blue Jay Steller’s Jay Rare No?
Carolina Chickadee Black-capped Chickadee Rare No
Tufted Titmouse Black-crested Titmouse Common Yes
Eastern Bluebird Mountain Bluebird Very rare* No
Rose-breasted Grosbeak Black-headed Grosbeak Various **
Speciation and Radiation

Indigo Bunting Lazuli Bunting Common Yes

Rufous-sided Towhee Spotted Towhee Common Yes
Eastern Meadowlark Western Meadowlark Rare Yes
Baltimore Oriole Bullock’s Oriole Common Yes

Source: Copyright © 1988 by Paul R. Ehrlich, David S. Dobkin, and Darryl Wheye.
*Only a single hybrid known.
**Common only along Platte River in central Nebraska; hybrids rare or unknown elsewhere;
well studied in only a few locales.

105

1stPages_A.indd 105 7/22/20 10:52 AM

 never been covered with glaciers. What to be both sedentary and habitat specific.
process has been causing allopatric Thus, few of the birds that remained
populations in this region to produce in the moist rainforest refuges adapted
such a vast number of bird species? It to arid habitats or moved across them.
appears that speciation in Amazonian Gene flow was stopped between rain-
forest birds is also related to climatic forest populations, and the speciation
fluctuations working in tandem with process could begin.
certain characteristics of tropical birds. With ameliorating conditions, the
Although these fluctuations are not isolated populations would follow the
as severe as glacial advances, they are expansion of the forests until the forests
equally effective in isolating populations. and birds made contact. At this time, the
Although the current Amazon basin normal possibilities could occur: sym-
appears to be a vast area of rainforest, patry through ecological and reproduc-
distinct variation occurs in rainfall tive isolation, parapatry, or hybridization
amount across this area. Pleistocene and interbreeding. If the birds followed
climatic fluctuations that caused tem- the expansion of the forests very closely,
perate glaciation were expressed in the we would expect an unusual number of
tropics by declines in rainfall, such that zones of contact or hybridization in the
long periods of arid conditions occurred. areas where the forests met, as occurred
During these dry periods, those areas
that now receive the most rainfall prob-
ably remained covered with rainforest,
while areas with intermediate rainfall Fig. 4.10. Estimate of where rainforest refuges
today developed arid scrub forests or occurred during glacial advances (dark green)
even savannas (fig. 4.10). As we will see and how these refuges relate to current
in more detail later, tropical birds tend rainforest distribution (Haffer 1969).
chapter 4

106

1stPages_A.indd 106 7/22/20 10:52 AM

 following glacial receding. Jürgen Haffer In the final stage (Stage IV), only one
(1969) has noted the possible forest ref- or two distinct species are left from the
uges that occurred during arid periods original set of populations. In either of
and those areas where it appears that the last two stages, a species could reex-
numerous populations made secondary pand, and if the ecological differences
contact. With several forest refuges and were adequate, this could result in two
several arid periods, we can see how the sympatric species. We are concerned
proper conditions for the evolution of a here with the taxon cycle only as a model
diverse avifauna occurred. for speciation, but Robert Ricklefs and
George Cox (1972) make some intrigu-
Speciation on islands ing suggestions about some of the
ecological and evolutionary mechanisms
Island systems often provide excellent that might drive this cycle in the West
examples of allopatric populations Indies.
that are undergoing speciation. On Although the taxon cycle concept
isolated archipelagoes, speciation of a might explain certain cases of speciation
single form may become quite com- within island systems, not all island
plex and lead to many different forms speciation events require adherence to
(see below). In the more typical case, a this cycle. Single colonization events
species may establish itself on several on islands have often led to species or
islands during a colonizing stage in its subspecies distinct from their mainland
life; these separate populations have ancestors. For example, pines on the
the potential for speciation, depending island of Hispaniola in the West Indies
on gene flow between islands and the support a race of the White-winged
conditions each population faces on its Crossbill (Loxia leucoptera) that is dis-
respective island. tinct from its mainland ancestors. This
The regular occurrence among does not represent the remnant of a
island birds of widespread populations widespread colonization event, however,
that undergo change and perhaps spe- but a single colonization. Given that no
ciation has led to the development of crossbills from the mainland ever visit
a concept known as the taxon cycle. It Hispaniola, in time this population will
has been suggested that at the start of undoubtedly be recognized as a separate
this cycle (Stage I), a population from a species.
source area has colonized a set of islands Other barriers can cause allopatric
and shows no variation between islands. populations of birds and initiate specia-
With time, each island population tion. Mountain ranges can do this for
Speciation and Radiation

should evolve characteristics best suited lowland birds; bodies of water might
to that island, such that interisland varia- separate coastal birds. Broad rivers such
tion appears. Stage II is often character- as the Amazon may be large enough
ized by recognition of subspecies among barriers to bird movement (especially
the populations. With the passing of tropical bird movement) to cause allo-
even more time, some populations may patry. In many cases, the Amazon serves
go extinct and those remaining may be as the boundary between the ranges of
considered separate species (Stage III). closely related species. If we look far

107

1stPages_A.indd 107 7/22/20 10:52 AM

 back enough in time, we can see how species provide, this island colonist may
the movement of the continents resulted develop a variety of forms in the way we
in allopatry and speciation. Other barri- suppose that primitive birds did during
ers could also work, even though birds early radiation. The conditions of an
are so mobile. archipelago allow both the isolation of
All the above examples of specia- populations and the colonization of new
tion events in nature follow the simple forms generated throughout the island
model for allopatric speciation that we system.
suggested earlier. While clear examples The classic examples of such insular
of successful speciation can be seen, we radiation occur in Darwin’s finches, the
must remember that speciation is in Geospizinae (which historically has been
many ways just a special case of evolu- considered a subfamily of the Ember-
tion. All populations are under the effect izidae or Fringillidae) of the Galapagos
of natural selection pressures that lead Islands, and the Hawaiian honeycreep-
to adaptive change, but the extent to ers of the Hawaiian Islands. This latter
which these changes affect reproductive group has been classified as either a
isolation is highly variable. family (Drepanididae) or subfamily
(Drepanidinae) associated with the
Radiation in Isolated Island Systems finches (Fringillidae) or the Australasian
honeyeaters (Meliphagidae).
It is apparent from the previous exam- Both of these island systems lie in
ples that we can construct reasonably tropical waters but are highly isolated
detailed models only for fairly recent from mainland sources of colonists. In
speciation events based on our knowl- both cases, scientists believe that one
edge of recent ecological conditions. We species has radiated into many different
saw earlier that most birds went extinct species with widely different ecologies,
about 65 million years ago, when an such that a single family dominates the
asteroid hit the earth. Most current birds songbird avifauna of the island system.
have evolved since then. We assume that This process of variation has occurred in
the great array of avian forms evolved just a few million years on these islands,
through allopatric speciation, but at a in contrast to the 65 million years
time when there were many more eco- during which modern birds have been
logical opportunities and a real chance evolving on earth.
for radiation (the evolution of new forms The Geospizinae of the Galapagos
to fill ecological niches). are perhaps best known because of
About the only exceptions to the their association with Darwin and the
pattern of limited changes in birds in theory of evolution. While this example
relatively recent times have occurred on may be well known, the extremely arid
certain isolated island systems. A bird conditions on most of the Galapagos
species colonizing an archipelago with Islands have resulted in rather limited
few other bird species or other types of opportunities for these species. The 13
chapter 4

competitors may have a wide variety of island species that presumably were
resources available to it. Without the derived from one form are dominated by
constraints that large sets of competing seed eaters (fig. 4.11). These are divided

108

1stPages_A.indd 108 7/22/20 10:52 AM

 into ground finches and tree finches, that the descendants of a seed-eating
with another small group specialized colonist evolved insectivory. Others have
for eating cactus fruit. Several of these argued that the Bananaquit (Coereba
“finches” have become insectivores, but flaveola) or its ancestor may have been
only two of them are highly modified the initial colonist. This widespread,
for this habit. One of these, the Warbler generalized nectar- and insect-eating
Finch (Certhidea olivacea), looks and bird is found on nearly every other trop-
acts like its namesake. Another makes ical island in the Western Hemisphere.
an attempt at being a woodpecker, but Since there are too few flowers on the
since it lacks the proper morphology for Galapagos to support a nectarivorous
pecking and probing, it has learned to bird, the bananaquit would have had to
use thorns as probing devices. shift to eating insects. Seed-eating forms
Although it is agreed that this variety would have evolved later. Many classifi-
of forms evolved from one original col- cation schemes suggest that the Warbler
onist, there is disagreement about who Finch is the most primitive offshoot of
the colonist was. Seeds seem to be much the main radiation of finches; because
more abundant and come in a wider this finch sings and builds a nest like a
variety on these islands than insects or bananaquit, it may be just a derivative of
flowers, so it is not particularly sur- the ancestral form. Other species from
prising that the avifauna is dominated the West Indies or South America have
by finches. Recent evidence points
to a mainland finch, the Blue-black Fig. 4.11. Radiation within the Darwin’s finches
Grassquit (Volatinia jacarina), as a pos- that resulted in several groups of species from a
sible ancestor.15 If this is true, it appears single ancestor.

Speciation and Radiation

109

1stPages_A.indd 109 7/22/20 10:52 AM

 been proposed as possible ancestors half-dozen different families by examin-
for Darwin’s finches. Although David ing the morphology of the bills. Unlike
Steadman (1982) felt so strongly about the dull finches of the Galapagos, the
his theory that he placed all of Darwin’s Hawaiian birds are often spectacularly
finches and the grassquit into the genus bright, especially those that feed at
Geospiza, this argument is far from over. flowers. Although the occurrence of a
Although not as well known as tubular tongue (an adaptation for nectar
Darwin’s finches, the Hawaiian honey- feeding) in all species suggests that the
creepers (Drepanididae) may serve as original colonist was a nectarivore, the
the best example of the radiation of one exact derivation of this group is still
form in a species-poor environment. argued. Recent systematic studies with
The climate of the Hawaiian Islands is DNA suggest that perhaps there are
much moister than that of the Galapa- two groups of birds in the Hawaiian
gos; thus the variety of habitats ranges radiation, with a small group of highly
from rainforest to alpine grassland. This adapted nectar feeders that resemble the
diversity of habitats and thus of foods, honeycreepers of the family Meliphagi-
including flowers, has led to an incredi- dae but are actually more closely related
ble radiation of forms. The bills of these to some temperate species such as
honeycreepers are extremely variable waxwings (Bombycillidae) and silky-fly-
(fig. 4.12), reflecting the wide variety of
foods these forms use. Fig. 4.12. Several groups of birds that
An inexperienced taxonomist might resulted from the radiation of the Hawaiian
place members of this family into a honeycreepers.
chapter 4

110

1stPages_A.indd 110 7/22/20 10:53 AM

 catchers (Ptilogonatidae) from the New radiated so dramatically. While mammals
World.16 It is suggested that five of the were also rapidly radiating at the same
Hawaiian species belong in their own time, flight allowed birds to fill a wide
new family, the Mohoidae, although all variety of ecological roles throughout the
the species in this family are extinct. world that mammals could not. In some
Whatever the source, the radiation of cases, the success of birds may have
the Hawaiian honeycreepers serves as been at the expense of more primitive
an excellent example of how a single reptiles and amphibians that were driven
species can radiate in a species-poor to extinction; in other cases it may have
environment. This is a miniature rerun been simply the expansion of a new form
of the sort of divergence going on in the that allowed use of resources that had
early history of birds; the occurrence of not been effectively harvested before.
this radiation only on extremely isolated Either way, it appears that a rather rapid
islands suggests how constrained the (in evolutionary terms) radiation must
speciation process is in the world today. have occurred such that all modern bird
groups had appeared by the Oligocene,
Long-Term Evolutionary Patterns 40 million years ago.
While it is difficult to speculate
The island examples of radiation are how allopatric populations occurred
of great value in showing us how one within continents so long ago, the recent
form could evolve into many different acceptance of continental drift does give
forms of birds given the proper circum- us some feeling for that phenomenon
stances and a few million years. Starting as a cause of allopatry. Inasmuch as the
with the first bird on earth, we assume separation of two continents could cause
a similar process gave us the diversity allopatry in forms originally found on
of birds we see today. Although avian both, and the shifting nature of water
paleontologists are hard at work, this barriers between continents affected col-
135-million-year process is still rather onization rates, knowledge of how and
poorly understood, particularly with when the continents drifted apart pro-
the mass extinction of 65 million years vides much insight into avian evolution
ago. Yet by looking at present-day bird in its early stages. These early radiations
distributions in light of what is known are important because the ecological
about other patterns of biology, geology, forms arising from them have been spe-
and climatology over the evolutionary ciating for many millions of years since,
history of birds, we can get some idea of and they are generally distinct enough to
what happened in the past. Basically, we be considered major taxonomic groups
Speciation and Radiation

need to review our knowledge of the eco- (families or orders) today.

logical conditions that were available to Geologists generally agree that the
birds over this time and the factors that single continent of Pangaea existed
might have promoted allopatric popula- until approximately 200 million years
tions, and thus speciation. ago, when it began splitting into Laur-
We assume that the evolution of asia (now North America and most of
birds was an adaptive breakthrough in Eurasia) and Gondwanaland (now South
the animal world at the times when birds America, Africa, India, Australia, and

111

1stPages_A.indd 111 7/22/20 10:53 AM

 Antarctica; fig. 4.13). This split occurred Fig. 4.13. Simple representation of how
well before the known occurrence of continental drift served to create allopatric
birds. At the time of Archaeopteryx at populations of many primitive birds.
the end of the Jurassic period, the conti-
nents occurred in three groups. Laurasia barriers between the oceans at that time.
was mostly intact and virtually in contact During the next 60 million years
with the combined masses of Africa and (135 to 65 million years ago), several
South America at what is now Gibraltar. major groups of primitive birds evolved.
The connected continents of Australia Laurasia remained intact and actually
and Antarctica lay at the southern end of increased its contacts with Africa, while
the world, slightly separated from South South America had split from Africa and
America–Africa. The subcontinent of moved westward. Antarctica-Australia
India was drifting northward by itself. remained in much its previous position,
Since climates at this time were gener- although this group was somewhat
ally mild, these continent groups may more isolated from other continents
not have differed greatly in ecological than previously. India continued its slide
conditions, and the gaps between them toward Asia, and Madagascar broke
were not great. We can already suggest, from Africa. The separation of Madagas-
though, that the continent pairs of North car at this time may explain the presence
America–Asia, South America–Africa, there of several apparently primitive bird
chapter 4

and Australia-Antarctica might share the groups that it shared with Africa before
most similarities of land bird forms. On separation but that have gone extinct on
the other hand, oceanic birds faced few the main continent since then.

112

1stPages_A.indd 112 7/22/20 10:53 AM

 Most modern birds evolved during most of the South American rainforest
the most recent 60 million years. After forms have extended northward only as
the massive extinctions of 65 million far as tropical forests occur. Yet in true
years ago, the continents continued to tropical rainforest in Central America,
shift toward the position in which we these “recent” South American forms
see them today, and in relatively recent are often the dominant species.
times, climates became more similar At this same time, the numerous
to what we presently experience. This geographic contacts between Africa and
climatic shift, and especially the ice Eurasia continued, such that barriers
ages that accompanied it, limited many to movement between the continents
formerly wide-ranging species to more were fewer and their avifaunas had
tropical climates, effectively isolating the probably become more similar with
tropical regions of the world. This shift time. In contrast, once Australia split
may also have spurred the evolution from Antarctica (which maintained its
of many species adapted to temper- polar position, became covered with ice,
ate climates on some continents. The and lost most of its fauna and flora),
split between North America and Asia it remained isolated and developed an
occurred fairly early in this period, such avifauna almost as distinct as its famous
that these continents have quite sim- marsupial mammals. Only in relatively
ilar avifaunas but a number of differ- recent times has Australia moved far
ent families that seem to replace one enough northward to exchange birds
another. This similarity has been aided with the islands of the Southwest Pacific
by several more recent connections and Southeast Asia.
between the continents over the Bering Although continental drift was
Strait of Alaska. The southerly portions the object of much controversy until
of North America produced a variety recently, zoogeographers have long
of distinctive tropical or subtropical accepted the existence of zoogeographic
groups; these met and mingled with the realms—areas with faunas distinct from
distinctive South American forms when those of other areas. Not surprisingly,
the Central American land connection these realms reflect the continental
was made a little less than six million movements outlined above, with the
years ago. At this time, a vast exchange least distinct realms occurring on those
of biota occurred, with some South continents that were least separated over
American forms expanding throughout history. For example, the continents
North America and vice versa. There that were formerly Laurasia are consid-
is much argument about which fauna ered by some to form a single zoogeo-
Speciation and Radiation

was the “winner” in this exchange. graphic realm, the Holarctic, although
North American mammals, especially others separate this into the Nearctic
carnivores, certainly seemed to domi- and Palearctic. The distinctness of the
nate and replace their South American Neotropical and Australian zoogeo-
marsupial counterparts. Many North graphic realms reflects their histories
American bird families have colonized of isolation, while the simplicity of the
the length of the Andes, especially in Antarctic zoogeographic realm reflects
high-altitude temperate habitats, while the devastating effects of a harsh cli-

113

1stPages_A.indd 113 7/22/20 10:53 AM

 mate on animals. The isolation of Africa Products of the Process:
has been accentuated by the location The Diversity of Avian Forms
of deserts and inland seas, such that
the Ethiopian realm does not generally The processes discussed above have led
include the north coast of that continent. to varieties of birds adapted to nearly
The only realm that does not reflect such all parts of the earth. Terrestrial forms
relatively simple continental movements live from ground level (and occasion-
is the Oriental realm, which consists of ally below) to high in the sky. Various
the tropical areas of South and South- aquatic forms have adaptations that
east Asia that have long been isolated allow them to go well below the water’s
by mountains from the more temperate surface; others search for food across
areas of Asia. The Oriental avifauna is the open seas. Birds use a wide variety
undoubtedly affected by the long-term of foods ranging from plants and plant
isolation of India and the islands of the products (fruits, seeds, nectar) to fish,
Southwest Pacific, but the smaller bar- mammals, and other birds.
riers between it and both the Ethiopian In the remainder of this chapter, we
and Palearctic realms make these realms will look at some of the general adap-
somewhat less distinct. And while each tations that have resulted from avian
of these realms can be categorized by radiation, beginning with the range
their distinct resident families or orders, of morphological traits that birds have
migration by thousands of avian species developed to move on the ground, in
causes seasonal blending of avifauna, as the water, or on other substrates (feet)
temperate species fly to the tropics for and to harvest foods (bills). We will see
part of the year and mix these historical how these modifications match up with
patterns in ways that are sometimes the flying options discussed in chapter
hard to understand. 3, and we will end with a brief look at
If we add all the above processes some of the rules that limit the size and
together, we can see that through the extent of some of these avian adaptations.
135 million years or so of avian specia- Although the uses of various types of bills
tion, populations have been in position and legs have been studied for centuries,
to become allopatric through a variety this study has become more sophisticated
of mechanisms ranging from conti- in recent years and has become known
nental drift to habitat change. To reach as ecomorphology. Ecomorphological
the nearly 10,000 species we see today research attempts not only to describe
has required a multitude of speciation the uses of various morphological traits
events. Systematists hope to unravel this in ecological terms, but also to explain
process by using what they know about such things as mechanical constraints on
the evolution of similar traits in birds, morphology, how different morphologi-
the speciation process, and historical cal characteristics affect one another, and
patterns of climate and geology. We will relationships between morphology and
look more closely at how they do this in behavior. Here we will avoid this com-
chapter 4

chapter 6; meanwhile, let us look at the plexity, while emphasizing the interaction
types of adaptations that have resulted between the ecology of a species and the
from radiation. morphology it has evolved.

114

1stPages_A.indd 114 7/22/20 10:53 AM

 Feet and legs Most birds that perch on branches
have the standard anisodactyl foot (fig.
The feet and legs of birds are generally 4.14). This is modified for birds that
adapted for perching and localized (non- climb on bark. In some cases this foot
flight) locomotion within the habitat may only be stronger, with a longer
where the bird lives. Adaptations may hallux or long, sharp claws. In other
aid in foraging or avoiding predators, species, the foot has become zygodac-
but in flying species the legs and feet tyl, with the outside front toe rotated so
cannot become so big as to hinder flight. that there are two toes in front and two
These appendages may also be useful in back. This presumably helps a bird
for scratching or for preening feath- “hitching” its way up a trunk. Two other
ers. The basic avian foot has three toes toe arrangements found in perching
pointing forward and one, the hallux, to birds are of less obvious value. A few
the rear. This is termed anisodactyly, but forms possess heterodactyl feet, with
much variation can occur in shape and two toes in front and two in back but
strength within this foot type. In some with the inside toe having rotated. In
species the toes have shifted to other syndactyl feet, the two inner toes are
arrangements to aid the bird’s activities. united for much of their length, result-
In many species, anisodactyl feet ing in a long, narrow foot.
have been adapted to the capture of prey. Small ground-dwelling birds gener-
Such feet (termed raptorial; fig. 4.14) have ally have strong, long-toed anisodactyl
long, strong toes with large, sharp claws. feet (fig. 4.14). On many, the hallux is
Often the claws can fold into the toe and considered incumbent, lying flat on the
the toes can be folded into a fist for a firm ground such that the sole of the foot is
grip on prey. Species that capture fish flat from front to back. In some of the
with their feet have special spiny scales larger ground dwellers the hallux may be
that aid in holding their prey. In a few elevated above the ground, and in some
forms the foot is formed into a fist that is of the largest running birds the hallux is
used to strike flying prey. absent. The toes and claws of the jacana
Aquatic birds are characterized by are unusually long and skinny, an adap-
feet with some form of webbing that tation for walking on lily pads and other
aids propulsion (fig. 4.14). The most aquatic vegetation.
extreme form of webbing is termed Full-time aerial insectivores tend
totipalmate, where all four toes are con- to have feet that are reduced in size
nected by webs. In palmate feet, only the and strength (fig. 4.14). In the swifts, a
three front toes are connected, although condition called pamprodactyly occurs,
Speciation and Radiation

the hallux may have a lobe on it to aid where all four toes face forward. This is
in swimming or diving. An alternative mostly an adaptation for hanging on to
form of swimming foot is termed lobate, walls while roosting.
where the toes have a series of lobes that Many other variations can occur
open when the foot is pushed backward. in the avian foot. Nails can vary from
Semipalmate feet are half-webbed and acute to obtuse to flattened or pectinate
may serve for occasional swimming or (having serrated edges). Some species
for walking on soft surfaces. that walk on soft sand or snow have

115

1stPages_A.indd 115 7/22/20 10:53 AM

 Fig. 4.14. Various types of bird feet. strong legs for running and sometimes
kicking. Some of the largest running
birds have only two toes.
broad toes and claws plus dense feather-
ing around the foot or rows of flat, wide Bills
scales.
The length of the tibia and tarsus For most bird species, the bill serves as
in the bird’s leg is also quite variable. a tool for capturing or finding food, as
Exposed portions of the leg are covered hands for picking food up, as jaws or
with a horny material whose structure teeth for shredding or crushing food
was once considered of taxonomic into smaller pieces, and as a mouth for
importance. Aerial insectivores tend to swallowing. In the feeding of young, it
have smaller legs than most birds, while may also serve as a basket for carrying
ground dwellers tend to have longer food. With such a variety of potential
chapter 4

legs. Some waders have extremely long, uses, it is not surprising that an almost
thin legs adapted for walking in water, infinite variety of bill types exists.
while large grazers have thick, extremely Flower feeders. Many species have

116

1stPages_A.indd 116 7/22/20 10:53 AM

 evolved adaptations for feeding on bill. Ideally, this restricts a particular
nectar in flowers, including tubular pollinator to a limited number of plant
or brush-tipped tongues for lapping species, which is best for pollination.
nectar. Because flowers are seasonal, Plant shape may also be variable, such
the diversity of nectar-feeding birds is that some plants deposit pollen on the
highest in the tropics. Because the New face of the pollinator, while others may
World and Old World tropical areas were brush the back of the head. Thus, while
separated fairly early in the history of bird-pollinated flowers have certain
the earth, these two regions have very traits in common (copious nectar, red
different families representing this color, tubular shape), not all pollinators
ecological group of birds (fig. 4.15). In can visit all flowers.
the New World, the flower-feeding guild Because nectar is such a reward,
comprises mostly members of the hum- some nectarivores have developed ways
mingbird family (family Trochilidae). to “cheat” these systems by poking a
Birds in this family are famous for being hole in the base of the flower with a
very small (as tiny as two grams), often sharp bill and then feeding on the nectar
brightly colored, and hovering at the from the side of the flower (see banan-
flowers they use for food. Some African aquit and flowerpiercer in fig. 4.15). This
sunbirds (family Nectariniidae) hover, circumvents the pollination advantages
but most do not, which is also true of the of the plant-pollinator mutualism,
other Old World nectar feeders, includ- so many plants have evolved ways to
ing the honeyeaters (Meliphagidae) and minimize their losses to such thieves.
flowerpeckers (Dicaeidae), although These may involve a very tough base to
nearly all flower-feeding birds have bril- the flower, nasty-tasting chemicals in the
liant plumage. Old World nectarivores flower, or a flower on a long, thin stem,
tend to be larger than hummingbirds, which is not reachable by larger nectar
in part because the flowers they visit are thieves that cannot hover.
also larger than those used by hummers Flesh eaters. Bills of carnivorous birds
in the New World. Old World nectar- are generally characterized by a sharp
ivores tend to perch at the base of the hook (fig. 4.16). Large carnivores use
flower to gain entrance to nectar. this hooked bill as a tool to shred prey
In this group, great variation in bill that is captured in the raptorial talons.
shape has evolved, primarily as a result Smaller carnivores such as shrikes
of coevolutionary relationships between (family Laniidae) and some of the larger
plants and pollinators. When a bird insectivores may use the hooked bill
visits a plant to get nectar, it also gathers itself to kill prey. Owls have fairly strong
Speciation and Radiation

pollen on its plumage, which the plant hooks to their bills, but this is hard to
hopes will be moved to another individ- see on their heavily feathered face. Car-
ual of that species for cross-pollination. rion feeders also possess a decided hook
Flower size and shape limit which spe- for tearing at flesh; this is often accom-
cies of pollinator can successfully visit panied by a bare head or face, as feath-
any given flower; for example, a straight ers would get matted with blood. The
bill does not fit into a curved flower, and hook is perhaps most pronounced in
a long, tubular flower requires a long species that specialize in eating snails,

117

1stPages_A.indd 117 7/22/20 10:53 AM

 Fig. 4.15. Bills of birds that harvest or few species use straight, sharply pointed
steal nectar from flowers. From left bills as spears. In species that catch fish
moving clockwise: Bananaquit (Coereba by plunging their head or whole body
flaveola), Scarlet-backed Flowerpecker beneath the water’s surface, the bill may
(Dicaeum cruentatum), Regent Honeyeater be quite heavy. Some of these forms have
(Xanthomyza phrygia), Masked Flowerpiercer a bill with serrations, apparently to help
(Diglossopis cyaneus), Handsome Sunbird
hold the fish. An unusual fish-catching
(Aethopyga bella), and Purple-throated
adaptation is the bill of the skimmer,
Mountain-gem (Lampornis calolaemus).
which has a long, knifelike lower man-
dible that cuts through the water until it
as it must be curved in such a way that finds a fish, which it grabs with its upper
it can penetrate the curved snail shell to mandible. Fish constitute at least a part
cut and extricate the snail body. of the prey captured by the sieving action
Fish eaters. A few of the fish-eating birds of spatulate bills or the extendable gular
that capture prey too large to swallow pouch of pelicans.
whole also have hooked bills for shred- Insect gleaners. The bills of birds that
ding their prey before eating it (fig. 4.17). feed on smaller insects and other
Other piscivores have bills adapted for invertebrates vary greatly depending
chapter 4

capturing, holding, and swallowing prey on foraging technique and habitat. The
items. Many of these bills are straight and standard insect gleaner that picks prey
are used as forceps for capturing fish. A off leaves and twigs has a short bill with

118

1stPages_A.indd 118 7/22/20 10:53 AM

 Fig. 4.16. Bills of birds that kill and eat an acute tip (fig. 4.18). Species that pick
Speciation and Radiation

meat. From left moving clockwise: American at buds or bark in search of prey may
Kestrel (Falco sparverius), Ornate Hawk- have a much stouter bill, while those
eagle (Spizaetus ornatus), Bearded Vulture that probe crevices may have a bill that
(Gypaetus barbatus), Snail Kite (Rostrhamus
is decurved. Decurved bills reach their
sociabilis), Brown Shrike (Lanius cristatus),
zenith in species adapted to foraging on
and Southern White-faced Scops-owl (Ptilopsis
tree trunks; several of these species have
granti).
enormous decurved bills to probe deep
into crevices. Other trunk foragers have

119

1stPages_A.indd 119 7/22/20 10:54 AM

 heavy, straight bills to scrape off bark, short, weak bill but a very broad mouth.
while species that drill into the wood Those that capture larger insects on
have chisel-shaped bills adapted for this the wing must have a broad mouth for
behavior. capturing prey but a heavy enough bill
Aerial insectivores. A variety of bill types to crush and eat it. These bills are often
are adapted to catch insects while birds hooked, but they differ from the hooked
are in flight (fig. 4.19). Species that bills described earlier by their breadth.
glean while hovering often have long, A few species specialized for catching
narrow bills for reaching prey without bees and wasps have long, compressed
getting too close to leaves or branches. bills that allow them to effectively catch
Birds that catch flying insects are char- and crush prey “at arm’s length.” Most
acterized by much broader bills, such species catching insects on the wing
that the opened mouth is a large insect have distinctive rictal bristles at the gape
net. Species eating small insects have a of the bill to aid in prey capture.
Small aquatic invertebrate eaters. Small
aquatic insects and other invertebrates
Fig. 4.17. Bills of birds that capture fish
are caught in a variety of ways (fig.
and other aquatic prey items. From left:
4.20). Certain birds of shorelines and
Double-crested Cormorant (Phalacrocorax
mudflats use their long bills to probe in
auritus), Common Kingfisher (Alcedo atthis),
Peruvian Pelican (Pelecanus thagus), Atlantic the mud and sand for prey items. The
Puffin (Fratercula arctica), Indian Skimmer bill tips in these forms are often very
(Rynchops albicollis), and Anhinga (Anhinga sensitive and may be flexible. Straining
anhinga). of small organisms may be done by
chapter 4

120

1stPages_A.indd 120 7/22/20 10:54 AM

 Fig. 4.18. Bills of birds that glean insects and is sharply bent; the bird forages with its
other small prey items from leaf, bark, or bill upside down while moving through
ground surfaces. From left moving clockwise: the water and sifting out food particles.
Groove-billed Ani (Crotophaga sulcirostris), In a few waterfowl species adapted to
Blue Nuthatch (Sitta azurea), Black-striped larger prey, the bill is still lamellate
Woodcreeper (Xiphorhynchus lachrymosus), but is much heavier and adapted for
Kaempfer’s Woodpecker (Celeus obrieni),
­crushing.
Raffles’s Malkoha (Rhinortha chlorophaea),
Fruit and seed eaters. Although a great
and Blue-winged Pitta (Pitta moluccensis).
many species eat fruit occasionally,
Speciation and Radiation

and many have diets that include large

amounts of fruit, very few are totally
narrow, recurved bills that are swept frugivorous. Because fruit is usually
through the water while rapidly opening soft, no great adaptations of the bill are
and closing; by long, depressed bills needed to harvest it. Most species that
armed with rows of lamellae; and by eat fruit also include seeds in their diet,
the unusual bill of the flamingo. This feed insects to their young, or have other
straining bill has extensive lamellae and alternative food types, and in most cases,

121

1stPages_A.indd 121 7/22/20 10:54 AM

 the bill shape is adapted to these non- usefulness in reaching hard-to-get foods,
fruit foods (fig. 4.21). Species that eat but it may also be an adaptation for
both fruit and seeds have two basic strat- eating nestlings, a common alternative
egies. Some simply swallow the food food. The distinctive bill shape of the
item and let the gizzard break it down. crossbill is a means of opening pine-
In these species, the bill is often simple cones to get the seeds.
and small, although the mouth may be
Fig. 4.19. Bills of birds that catch insects in
modified so that it can expand and swal-
the air, either from perches or by continual
low very large food items. Other species flying and searching for prey. From left
are adapted to husk or crack large food moving clockwise: Turquoise-browed Motmot
items before they are swallowed. The (Eumomota superciliosa), Barn Swallow
most developed of these have extremely (Hirundo rustica), Common Nighthawk
heavy bills, with or without a hook. This (Chordeiles minor), Chimney Swift (Chaetura
form grades into species with smaller, pelagica), Coppery-chested Jacamar (Galbula
more conical bills adapted for smaller pastazae), Asian Paradise-Flycatcher
seeds. The adaptive value of the bill of (Terpsiphone paradisi), and Puerto Rican Tody
the fruit-eating toucan may reflect its (Todus mexicanus).
chapter 4

122

1stPages_A.indd 122 7/22/20 10:55 AM

 Fig. 4.20. Bills of birds that feed along shores more in the digestive tract than in the
and capture mostly small invertebrates bill.
or fish. From left: Long-billed Curlew
(Numenius americanus), American Avocet Wings, tail and body: The final package
(Recurvirostra americana), Saddle-billed
Stork (Ephippiorhynchus senegalensis),
We earlier discussed various types of
Wood Duck (Aix sponsa), Caribbean
flight and the wings and tails associated
Flamingo (Phoenicopterus ruber), American
Oystercatcher (Haematopus palliatus),
with these. This set of options must be
Eurasian Spoonbill (Platalea leucorodia), and added to the available bill, foot, and leg
types when constructing the final bird,
Speciation and Radiation

White Ibis (Eudocimus alba).

with the body shaped to fit all the com-
ponents. Although a look at the Dodo
(Raphus cucullatus) might suggest other-
The bills of the relatively few species wise (fig. 4.22), the components are not
that eat much green plant material show mixed together haphazardly. Rather, the
no general pattern of shape. A few are occurrence of certain bill and foot types
depressed and lamellate, but the adap- is highly correlated with certain flight
tations of these herbivores seem to be patterns. A bird with raptorial feet for

123

1stPages_A.indd 123 7/22/20 10:55 AM

 capturing prey usually has a hooked bill idea of the ecological stresses on various
for tearing the prey while eating. Birds types of birds by looking at variation in
with bills adapted for catching flying size within each type. Earlier we pointed
insects usually have wings adapted for out how wing-to-weight ratios limit
the proper form of flight. Long-legged the ultimate size of flying birds, but
birds usually have a bill or neck long only a few species even approach these
enough to allow the bill to touch the mechanical limits. Among these are
ground.
The existing structures of birds are
Fig. 4.21. Bills of birds that specialize on
the result of an agelong process of evolu-
eating fruits and seeds. From left moving
tionary compromises that have favored
clockwise: European Goldfinch (Carduelis
those species adapted to available envi-
carduelis), Rose-breasted Grosbeak (Pheucticus
ronmental conditions. These conditions ludovicianus), Red Crossbill (Loxia curvirostra),
sometimes favor specialization, but at Toco Toucan (Ramphastos toco), Orange-
other times they favor generalization. In breasted Pigeon (Treron bicinctus), Araripe
most cases, food is the chief limiting fac- Manakin (Antilophia bokermanni), Golden-
tor, but nest sites, roosts, or other factors hooded Tanager (Tangara larvata), and Black-
can also be important. We can get some headed Parrot (Pionites melanocephalus).
chapter 4

124

1stPages_A.indd 124 7/22/20 10:56 AM

 carnivores, scavengers, and some large finding greater amounts of food. Hum-
herbivores, all of which can feed on mingbirds can be as small as 2 g, but
abundant or large prey items. The larg- they must use a variety of physiological
est of these are assisted by well-devel- tricks to survive at this size (see chapter
oped soaring behavior. More frequently 8). The smallest birds other than hum-
among birds, the size and quantity of mingbirds are about 5 g, a size limit that
available food may serve as an upper occurs in several different bird groups.
limit to size long before any mechanical Warm tropical regions have many spe-
constraint of flight. Flower feeders such cies this size, but temperate areas have
as hummingbirds and sunbirds that few. Of these, only the kinglets (Regu-
hover in front of flowers pay such a high lus) regularly winter in the north, and
energetic cost for this behavior that they these are distinctive for their very heavy
must be small; the largest hummer is coat of feathers and propensity to roost
only 20 g, and most are less than 5 g. in small groups.
Aerial insectivores are generally small The factors involved in combin-
because their foods are small, while fish ing all these morphological traits as a
eaters with similar body design can be response to the ecological pressures that
much larger. birds face are still being studied. We are
At the bottom of the size gradient, just beginning to understand the “rules”
a species must compensate for the for the construction of a particular bird
high metabolic cost of being small by through ecomorphological studies.

Speciation and Radiation

125

1stPages_A.indd 125 7/22/20 10:56 AM

 CH A P T E R 5

Constraints on
Avian Diversity

T
he term “diversity” refers to distribution, on both local (termed com-
the number of species living in munity structure) and regional scales.
a designated area. The sim-
plest measure of diversity is a Are There Constraints
count of species, but quite sophisticated on Avian Diversity?
indices of diversity have been developed
that try to measure both the number Although speciation itself is highly bio-
of species in a location and the relative logical, many of the factors that promote
number of individuals of each species it are not. For example, the occurrence
in the group. The study of groups of of glacial patterns or climatic cycles has
coexisting species is generally a part of nothing to do with the biology of the
community ecology, a science that tries species that might be affected by these
to understand the factors that affect the events. Species might vary in how they
number and types of species that can respond to these factors; for example,
live together in different ecological situa- a tropical species with high mobility
tions across the world. might not develop allopatric popula-
To understand the evolution of bird tions during the isolation of rainforest
communities, we begin with the simple reserves and thus not develop new
model for bird speciation discussed in species, but this cannot be considered
chapter 4. Going from one bird species a response to these climatic conditions.
in a location to two species requires two Given the importance of such climatic
processes: reproductive isolation to give events in speciation, we could envi-
us the two species, and ecological iso- sion two areas of differing topographic
lation to allow them to live together. To complexity (one with very homogeneous
generate a full community of species, we vegetation and climate and the other
must envision how this process might with very heterogeneous conditions)
work repeatedly over long periods, keep- that differ in the number of species they
ing in mind the various factors, both contain purely because of the number
biological and nonbiological, that might of times that climatic or other events
promote or constrain reproductive and have allowed speciation to occur in the
ecological isolation. In this chapter, we topographically complex area. In other
will look at how these factors might words, the difference we would see today
interact in determining patterns of bird in the diversity of species found in these

126

1stPages_A.indd 126 7/22/20 10:56 AM

 two locations (with more species in the of circumstances. Since most species
area of topographic and climatic com- have had their ecological fates decided at
plexity) could be explained by chance some previous time, we are often faced
events during the history of these areas. with looking at the so-called ghost of
We have already mentioned that the competition past. We see the results of
second mechanism leading to increased competition for resources in the differ-
avian diversity, ecological isolating ences between coexisting species or in
mechanisms resulting from competi- the displacement patterns of similar
tion between species, is a controversial species, but we do not always see the
subject. While no one doubts that the interaction itself at work today.
evolution of new species often involves Given the varying importance that
changes to new foods or foraging behav- different scientists attach to the mech-
iors, there is disagreement over the anisms of reproductive and ecological
extent to which species change into these isolation in determining diversity, a
new forms because the new ecological whole gradient of models describing the
areas they are using were previously evolution of the world’s birds could be
unused, or because their old ecological developed. Let us look at three models,
niches were full. In the former case, each of which represents a different
the new species can be thought of as point on this gradient.
jumping into this new adaptation, while
in the latter case it can be thought of as Speciation rates determine diversity
being pushed into it by its competitors.
The extent to which new species jump The first model suggests that ecological
into making changes compared to being interactions among species have little
pushed into them undoubtedly depends to do with the number of species living
on a number of factors, but chief among in the world today. Rather, this num-
them is probably the number of other ber reflects solely the rate at which the
species with which the species under sorts of events that lead to allopatric
consideration live. In an environment populations have occurred and have
with few species and much open envi- thus provided conditions for speciation.
ronmental niche space, we might see While the extinction of existing species
much jumping to new niches; when is allowed under this model, it is gener-
there are many species in a habitat, the ally felt that this extinction is the result
idea of a species being pushed into a of interactions between each species and
Constraints on Avian Diversity

remaining open area, perhaps a special- its environment, not the result of inter-
ized one, seems more likely. Competition actions with other species.
between species should certainly be more To understand present diversity
pronounced in the latter case as a result patterns using such a model, we would
of what ecologists call a relatively satu- look primarily at patterns of climate and
rated environment. vegetation in the past that could have
Measuring the extent to which inter- favored speciation. Areas with favor-
specific interactions led to the ecological able conditions for speciation would
differences we see among most species be expected to have more species than
today would be difficult under the best those with less favorable conditions (as

127

1stPages_A.indd 127 7/22/20 10:56 AM

 suggested above). Although ecological Moderate amounts of ecological control
factors would put some limits on diver-
sity (we would not expect a fruit-eating The third, intermediate model suggests
species if there were no fruit), the domi- that either speciation rates or ecological
nant factor in explaining diversity under controls may sometimes have some
such a system would be history. effect on species diversity or community
structure. Ecological interactions such
Ecologically fine-tuned bird distributions as isolating mechanisms limit to some
extent the types of species that coexist
At the other endpoint of our gradient of in a habitat, which means that historical
models is one that is very deterministic. factors are not the sole determinant of
This suggests that habitats are saturated diversity. On the other hand, the groups
with species; that is, there are more of species that coexist seem to respond
species attempting to live in a particular to such environmental factors as climate
location than can coexist there for any as much as to one another, such that
length of time, such that the number tightly structured communities may not
actually existing is a maximum given occur.
resource conditions, population charac- In this model, we would expect that
teristics, and so forth. A large number of interspecific interactions such as compe-
species may coexist where resource lev- tition occur on occasion, but that most
els and other factors allow fine ecologi- of the time coexisting species behave
cal isolating mechanisms; fewer species independently of one another. Depend-
would be expected where resource levels ing on the frequency of the climatic or
and/​or climatic factors require greater other events that cause the occasional
differences among species for their interspecific interaction, we might see
survival. elements of community structure in
Obviously, the diverse, complex, the types and numbers of species that
highly structured communities sug- coexist, but not in the relative densi-
gested here cannot exist without ade- ties of each. For example, if one of two
quate amounts of speciation to provide similar species competitively excludes
enough species to fill them. This model the second during these climatic events,
suggests that enough species have we should never expect to see the second
evolved in the past that speciation is species in this habitat unless the col-
no longer a limiting factor. Rather, the onization rate of the second species is
interactions among those species that greater than the frequency of the limit-
exist and new ones being generated ing climatic event.
determine which species survive within
the highly structured communities we Is there a correct answer?
see. Thus, there could be an equilibrium
between the rate at which new species If we asked 30 ornithologists to select
are generated through the speciation the point on the above gradient that they
chapter 5

process and the extinction of species felt represented the balance between
because of ecological factors within speciation factors and ecological factors
these saturated environments. in determining avian diversity, we might

128

1stPages_A.indd 128 7/22/20 10:56 AM

 get 30 different points. To the extent that found in this habitat over a given period.
these ornithologists worked in different Scientists favoring less extensive
locations across the world, they might all ecological control of bird communities
be correct. Is it surprising that a group often work in either seasonal or highly
of organisms that live in nearly every variable environments.1 Examples
habitat across the earth should show include temperate-zone habitats such as
great diversity in terms of the relative grasslands and arid shrub-steppe, and
importance of historical factors, such as such tropical vegetation as thorn-scrub
speciation, and ecological factors, such and savanna.
as competition, in determining the com- It is harder to find evidence favor-
munities that can live in particular sites? ing a purely historical explanation for
Although tropical rainforests can diversity, but this may reflect the state
support a great diversity of species (see of our knowledge of bird communities
below), many of these species include as much as anything. Until we better
sedentary individuals that may live in understand patterns of avian community
the same territory for life. The stable, structure, we will not be able to point
gentle climatic conditions of rainforests out situations where it appears that
allow most birds to survive long periods, species are absent because of historical
as do the predictable amounts of such factors affecting speciation. Yet some
resources as food and shelter. It is not distributional anomalies suggest that
surprising, therefore, that most studies history can be of great importance. For
of birds in these habitats find consistent example, Australia seems to have fewer
patterns of species distributions that gleaning insectivorous birds than other
can be explained to a great extent by areas, perhaps because the proper forms
interactions among coexisting species did not evolve. Lizards seem to fill these
(including interactions among birds and niches instead. The New Guinea region
other animals or plants). Although a is distinct in having a number of large
lush tropical island might contain fewer avian fruit eaters, which might occur
species, there, too, a highly interactive only because this area lacks the arboreal
model for the evolution of communities monkeys that normally fill this niche
could be appropriate. in other tropical areas. Small islands or
Contrasting situations would isolated habitats are other areas where
occur in habitats where environmental we might see that either speciation or
conditions were less stable, such that colonization rates are limiting the diver-
Constraints on Avian Diversity

populations of birds and levels of their sity of birds living there.

resources were not always synchronized. Few ecologists feel that the diver-
Following some severe climatic condi- sity of birds on earth is a product solely
tion, bird populations might fall below of historical patterns of speciation.
available food or other resource levels, Rather, most feel that this diversity is
perhaps for a long period. Because the product of speciation rates and a vast
different species might respond to both array of interactions that determine the
the climatic constraint and the period success of coexisting species. Depending
following it in different ways, we might on the habitat, the population levels of
see great variation in the community the species involved, climatic patterns,

129

1stPages_A.indd 129 7/22/20 10:56 AM

 and so forth, interactions among spe- Advantages of islands and
cies may be more or less important in the equilibrium model
determining the types and numbers of
species that coexist and, in some way We have already seen how the isolated
or other, give a community structure. simplicity of such island groups as the
Some of the controversy over the degree Galapagos and Hawaii has made them
to which interactions determine com- excellent locations in which to study
munity structure has been the result of speciation and radiation. Unfortunately,
differing definitions. Some scientists the distinctiveness of these islands
feel that finding the same set of species seems to limit their usefulness in stud-
in different areas with the same type of ies of community structure, primarily
vegetation shows that there is commu- because their avifaunas are very small
nity structure; others require not only and evidence suggests that the plants
the same set of species but identical and insects on which these birds feed
densities of each species to meet their are unusual in their own right. For more
requirements for a structured commu- meaningful studies on bird community
nity. As we look at studies of patterns in structure, we turn to tropical island
bird communities, keep in mind how systems that are close enough to main-
the variation in strength of the various land areas to have relatively large bird
causative factors might affect the compo- communities and habitats similar to
sition of these communities. Given that those on the mainland. Ideally, this con-
all our models suggest some ecological sistency in habitats results in the main
constraint on the existence of bird spe- variable from mainland to island being
cies (a fruit-eating bird cannot live with- the number of coexisting bird species,
out fruit), the following material sup- although in some cases this assumption
ports all models to some degree. From of resource consistency may fail.
the following evidence or any other that The first pattern of apparent orga-
is available, we can decide which of our nization that appears for any group of
models is most appro­priate. organisms in an island system is the
species-area curve (fig. 5.1). Large islands
Island Patterns of Bird Communities will contain more species than small
islands in virtually all cases within a
If community ecologists had access general geographic area. Much of the
to a time machine, they might be able remaining scatter in the species-area
to understand the evolution of a bird relationship may be due to the effects
community by going back in time to the of island isolation. An isolated island
point where there were only 10 species will generally hold fewer species than a
in a habitat, then 20, 30, 100, and so like-sized island that is closer to a bigger
forth. Unfortunately, this method is island or the mainland.
presently unavailable. Perhaps the next While the species-area regression is
best way to look at how bird commu- generally a tight relationship within an
chapter 5

nities are assembled is to examine the island system, the slope of this regres-
distributions and ecology of island birds. sion may vary from place to place. For
example, the islands of the West Indies

130

1stPages_A.indd 130 7/22/20 10:56 AM

 Fig. 5.1. Species-area relationships for land Although the species-area phenome-
birds of the West Indies (top) and Southwest non has been known for a long time, our
Pacific (bottom). The West Indies is composed understanding of the apparent mech-
of oceanic islands only, whereas the Southwest anism causing this relationship took a
Pacific contains oceanic islands and land- giant step forward with the equilibrium
bridge islands (red dots). Note that the largest model of island biogeography developed
land-bridge islands contain more species than
by Robert MacArthur and E. O. Wilson
Constraints on Avian Diversity

similar-sized oceanic islands.

in 1963 (fig. 5.2). They felt that the num-
ber of species on an island (termed S)
add relatively fewer species with increas- is the result of an equilibrium between
ing area compared to those of the South- two processes: (1) the immigration (or
west Pacific (fig. 5.1). These differences colonization) rate at which new species
may reflect basic variation in the environ- become established on an island, and
ments provided on the islands, particu- (2) the extinction rate, which measures
larly the foods available (see below), or loss of species on the island. After some
they may reflect historical differences in period, this dynamic system should
speciation or extinction rates. reach an equilibrium where every loss

131

1stPages_A.indd 131 7/22/20 10:56 AM

 of a species is balanced by an addition, islands that were once coastal highlands
or vice versa. It is expected that large during periods of lowered ocean levels.
islands would show higher colonization When the oceans rose, these highlands
rates because they are a bigger target became islands but initially held species
and have more space to hold species. densities comparable to those of main-
The situation is reversed on small land areas. Through extinction of many
islands, and they undoubtedly show species, these island avifaunas have
higher extinction rates because of their “relaxed” to more island-like levels (fig.
size. Increasing distance from sources 5.1), although some large land-bridge
of colonists would tend not only to lower islands have not lost all the species we
the colonization rate of an island but might expect in the years since they
also to raise the extinction rate because became islands. Recent examples of
new colonists would not be able to help species losses on islands have occurred
declining populations avoid extinction. on human-made islands, such as those
Different curves for near or far and large formed by Gatun Lake, the major part
or small islands result in different equi- of the Panama Canal.2 Barro Colorado
librium species numbers (fig. 5.2). Island, the largest island in Gatun Lake,
Support for this model has come in appears to have lost nearly 20% of its
various forms. Both natural disasters original forest avifauna in the last 90
and human activities have caused the years, despite being a nature reserve.
defaunation of whole islands. These Finally, support for the dynamic nature
islands were eventually observed to of the model has come from studies on
regain species until equilibrium was turnover, where changes in the compo-
achieved (fig. 5.1). In other cases, islands nent species of an island are observed
that were supersaturated with species even though no major change in total
have been observed to lose species species number occurs.3
until equilibrium was achieved. The Given a dynamic system like the
best examples of this are land-bridge above functioning over a long period,

Fig. 5.2. The simplest

form of the MacArthur-
Wilson equilibrium
model, which suggests
that the number of
species on an island (S)
is a dynamic balance
between the rate of
colonization and the
rate of extinction on that
island.
chapter 5

132

1stPages_A.indd 132 7/22/20 10:56 AM

 we would expect that each island would species found on New Guinea, which
eventually accumulate those species can be considered a mainland in most
most compatible with the conditions of ways. Among the islands are both
that island and each other. After equi- land-bridge and oceanic islands, which
librium has been reached, turnover of a allows comparison of islands where all
species should occur only when a “bet- birds had to colonize with those where
ter” species replaces a species already on communities remained from previously
the island. If this is the case, fairly rigid more complex avifaunas. Difficulties
patterns of community organization arise in searching for patterns in such
might be expected on these islands; if diverse communities. In the West
interactions among species are not so Indies, the simplest patterns occur on
important, this should not be the case. islands with fewer than 40 land bird
Let us look at some specific examples to species. Larger islands provide more
see whether repeatable patterns in the obscure patterns. Such small commu-
assembly of bird communities seem to nities are uncommon in the Southwest
be occurring. Pacific, while large communities prevail.
To search for patterns within this
Southwest Pacific island bird complexity, Jared Diamond (1975)
distributions separated species into guilds that are
more distinctly defined than those in
The area of the Southwest Pacific includ- the West Indies. For example, while all
ing New Guinea, Indonesia, the Philip- West Indian pigeons were considered
pines, and northern Australia includes frugivores and combined in a guild with
many more islands and more large thrashers and finches, Diamond was
islands than the West Indies. The spe- forced to divide the large pigeon family
cies-area curve for this region is steeper of this region into separate guilds. Most
than that of the West Indies (see fig. 5.1), distinct of these are the fruit pigeons, a
such that many islands within groups group set apart by modified intestines
like the Solomons and Bismarcks con- that force them to feed only on soft
tain well over 100 species, compared to fruits. Other distinct guilds that he exam-
a maximum of 70 species in the West ined include cuckoo doves, gleaning
Indies. The Pacific islands also seem flycatchers, and myzomelid-sunbird nec-
more dynamic than the West Indies. Size tarivores. Thus, Diamond examined the
shifts within a species are rare in the distributional pattern of some distinctly
Constraints on Avian Diversity

Southwest Pacific; rather, it appears that similar guilds of birds, but not the whole
community structure patterns are formed community, as we will examine later.
by the selection of appropriate coloniz- What Diamond proposed are
ing species from the many wide-ranging “assembly rules” of guild structure that
species available in the region.4 allow certain combinations of food hab-
This complexity has both advan- its and sizes to occur on some islands,
tages and disadvantages. The number but not on all islands. In the case of
of islands and the variation in their size fruit pigeons, size seems to be a central
provide an almost continuous gradient parameter, such that like-sized guild
in community size to the nearly 400 members cannot coexist on any but the

133

1stPages_A.indd 133 7/22/20 10:56 AM

 Fig. 5.3. Assembly rules for the fruit pigeon which of a set of similar-sized species
guild on Southwest Pacific islands ranging might occur on a particular island,
from as large as New Guinea (top) to small
resulting in some spectacular patterns of
(bottom). Note that like-sized fruit pigeons
distribution called checkerboard pat-
never coexist, and the separation between
terns (fig. 5.4), the underlying structure
coexisting sizes increases as islands get smaller.
seems to be determined by interactions
between species. These distributional
studies have been supported by evidence
largest islands (fig. 5.3). In other guilds, of niche shifts and turnover.6 Although
habitat specialization or other factors are the complexity of these islands has kept
important. Once again, these patterns anyone from figuring out the simplest
of structure appear to make the guilds rules at work, the evidence strongly sug-
resistant to the invasion of new species gests that interactions between ecologi-
while allowing the existence of guild cally similar species are a critical part of
members. determining the structure of Southwest
There has a been a great deal of Pacific island bird communities. Recent
controversy about whether these pat- modeling that took advantage of mod-
chapter 5

terns could have been generated by ern computer capabilities showed the
chance.5 Although it appears an element extremely nonrandom nature of these
of chance is involved in determining checkerboards.7

134

1stPages_A.indd 134 7/22/20 10:57 AM

 Fig. 5.4. A checkerboard pattern for small types cover most islands. Dry or sclero-
honeyeaters in the Bismarck Islands. Only one phyll forest is found in lowland areas,
species occurs on each island, but this may be particularly in rain-shadow situations.
one of five different species. This scrubby, thorny vegetation includes
many cacti and is nearly leafless during
the December–May dry season (fig. 5.5).
Lush, often tall rainforests occur on the
Patterns in West Indian bird windward sides of islands and moun-
communities tain slopes. Although these vegetation
types differ dramatically in composition,
The West Indies constitutes a set of botanic studies have shown that the
tropical islands situated more or less species composition of each type is very
between North and South America. The consistent from island to island through-
Greater Antilles are large islands run- out the West Indies. This suggests
ning east and west from near Florida that the resources available within the
into the Atlantic. The larger of these are habitats should be fairly consistent from
Constraints on Avian Diversity

mountainous, with peaks on Hispaniola place to place. Because most islands are
exceeding 10,000 feet. The Lesser Antil- composed of these two major habitat
les are a string of much smaller islands types, studies have focused on patterns
running north and south from near of bird community structure within
South America to the eastern end of the these habitats on islands of varying size
Greater Antilles. The Lesser Antilles are and with varying habitat proportions.8
mostly volcanic islands, although a few The West Indies shows a typical
were formed by uplifting of limestone. species-area relationship for its land bird
Large islands in the West Indies fauna (excluding hawks and owls; see
contain many vegetation types, but two fig. 5.1). Most of the scatter within this

135

1stPages_A.indd 135 7/22/20 10:58 AM

 relationship can be explained by differ- fruit- and seed-eating species, nectari-
ences in isolation of the islands. Habitat vore for nectar feeders, gleaning insec-
complexity per se seems to have little tivore for species that catch insects on
effect on species number. surfaces while perching, and fly-catching
A species-area relationship would be insectivore for those that catch insects in
expected even if the species involved did the air after flying from a perch. Rela-
not interact in any way. To see whether tively few West Indian land birds do not
these island communities are struc- fit into these guild designations.9
tured by any interspecies interactions, The number of species in a guild
we must look for further patterns of could be plotted against island area, and
distribution and competition. Follow- significant correlations would appear
ing the lead of Diamond’s work in the (as in fig. 5.1). The total number of
Southwest Pacific but recognizing that species in a guild could also be plotted
the West Indies supported smaller bird against the total number of species on
communities, other researchers split the island (fig. 5.6). The logic here is
the total species lists for each island into that equilibrium community size is the
guilds, sets of species with similar diets critical factor in patterns of community
and/​or foraging habits. The simple guild structure. Although this equilibrium
designations used were frugivore for all is the result of area and isolation, we
might expect similar ecological stresses
Fig. 5.5 a and b. Tropical dry forest (left) and on 20-species communities despite their
rainforest (right) in the West Indies. Photos by occurrence on different-sized islands.
John Faaborg. Within the West Indies, all that this
chapter 5

136

1stPages_A.indd 136 7/22/20 10:58 AM

 manipulation does is reduce some of the appeared. First, as the researchers sur-
scatter resulting from isolation effects; veyed birds within habitats on islands of
extending this approach to other islands increasing size, they noted that a level of
produces some unusual results (see apparent species saturation was reached
below). Plotted either way, these guild (fig. 5.7).10 The largest West Indian
membership versus area or total spe- islands had no more species living
cies regressions show highly structured within a habitat than the medium-sized
assemblages of bird species on West islands. This saturation number of
Indian islands. This suggests that the species was higher in dry forests than in
equilibrium species number of an island wet forests and occurred for both total
is a stable assortment of members of lists and guild membership lists. This
various guilds. means that the larger species lists of
This study next looked for patterns large islands are not accomplished by
of structure within these guilds on the fitting more species within a habitat, but
islands involved. Two intriguing patterns by having greater differences between

Fig. 5.6.
Regression of
the number of
species within
each foraging
guild on a West
Indian island
and the total
land bird species
on that island.

Constraints on Avian Diversity

137

1stPages_A.indd 137 7/22/20 10:59 AM

 habitats in species composition and by such as 3 g, 6 g, and 11 g nectarivores, 11
having a greater number of habitats. On g, 22 g, and 45 g flycatchers, and 9 g, 18
a guild basis, these saturation patterns g, 36 g, and 72 g frugivores. These are
meant that there were never more than the Hutchinsonian ratios mentioned in
two or three nectarivores or flycatchers, chapter 4; while there has been much
four to six gleaners, and seven to nine controversy over whether such ratios are
frugivores coexisting within a habitat. real and what function they serve, they
Because mist netting was used as a are common within these West Indian
sampling tool, a variety of morphological bird communities.12 Only among the
measures were made of captured birds. frugivores living on large islands do
It was discovered that coexisting species similar-sized guild members coexist; in
within the guilds were almost always of these cases, more complex ecological
different sizes (fig. 5.8).11 Sequences of isolating mechanisms seem to be at
coexisting guild members regularly con- work.
sisted of approximate doublings in size, Support for the dynamics of these

Fig. 5.7. Saturation curves in

the West Indies show that
there is a limit to how many
guild members can coexist in
a similar habitat type on a
West Indian island.
chapter 5

138

1stPages_A.indd 138 7/22/20 10:59 AM

 patterns is found in two ways. Several with the result that bird communities
cases exist of species that are different are resistant to extinction of present
sizes on different islands (character forms and also resistant to invasion of
displacement) to fit into the appropriate new forms. While some characteristics
size sequences. The West Indies had of these distributional patterns show the
many cases of checkerboard patterns, as effects of chance and some important
seen in the Southwest Pacific. In these effects of history, the above patterns
cases, a guild would show similar-sized support a very interactive, competitive
members from island to island, but the
species filling this spot would vary. Fig. 5.8. Mean weights of all members of
The above examination of bird char- various guilds in dry forest habitats (top) and
acteristics in the West Indies suggests wet forest habitats (bottom) on twelve West
strong patterns of structure among these Indian islands: (a) fly-catching insectivores; (b)
island communities. A set of ecological gleaning insectivores; (c) frugivores; and (d)
“assembly rules” seems to be at work, nectarivores. From Faaborg (1982).

Constraints on Avian Diversity

139

1stPages_A.indd 139 7/22/20 10:59 AM

 model for the assembly of West Indian mediate between the West Indian sites
bird communities. in the number of land bird species that
eat seeds. The maximum dimension of
Variation in tropical island patterns the available fruits and seeds occurring
on these sites was measured and seed
In the preceding material we described size frequencies plotted (fig. 5.9). Santa
some patterns in bird communities on Fe has a highly skewed seed size dis-
two island systems. Earlier, we looked tribution, with essentially nothing but
briefly at Darwin’s finches on the Gala- small seeds. Both West Indian locations
pagos Islands; since they constitute the have a much larger mean seed size and
majority of land bird species on that a greater range of sizes; even tiny Mona
archipelago, they may be thought of as Island provides a set of seeds similar to
a community. Certain patterns seem to those in similar habitat in Puerto Rico.
appear on all these islands; for example, Given the correlations that exist
size differences between coexisting guild between bird size and food size, we can
members are a regular occurrence. Yet make some predictions about the bird
differences occur between these island communities that these various seed
systems in the amount of size difference sizes should support. Santa Fe should
that seems to be important and in other not support frugivores as large as those
characteristics of their bird communi- of the West Indies; large food is just not
ties. Evidence suggests that these dif- there. Coexisting frugivores on Santa Fe
ferences may arise from differences in that attempt to isolate by body size, and
the resources available on these islands. thus food size, will be forced to live with
As we mentioned earlier, resources will smaller differences in size, or else fewer
limit avian diversity whether or not com- species will coexist. We would expect the
petition is, as many believe, important in West Indian sites to have a larger variety
structuring communities. What can we of bird sizes. This should be true even
say about the cause of this variation in on Mona, which provides a range of
community structure across the world? food sizes similar to that on Puerto Rico.
Studies of the available resource Characteristics of the frugivorous
base are difficult, but some interest- birds living on these islands match the
ing clues to resource variation can be resource traits. The largest fruit eater in
found by looking at the sizes of fruits the Galapagos is much smaller than that
and seeds available on different islands. of the West Indies sites (fig. 5.10). Coex-
These can be compared to the sizes isting congeneric Darwin’s finches differ
of fruit- and seed-eating birds on the by body size to a smaller degree than
various islands. Specifically, two West found in the West Indies but seem to
Indian locations (the Guanica forest of have accentuated differences in bill size
southwestern Puerto Rico and Mona with increasing body size, which sug-
Island) have been compared with a gests that the hardness of seeds selected
Galapagos Island (Isla Santa Fe) in is more important in species separation
chapter 5

terms of available seed sizes. All these than seed size.13 The tiny Mona Island
locations share similar climates and frugivore community consists of four
vegetation forms, with Santa Fe inter- species of different sizes (compared to

140

1stPages_A.indd 140 7/22/20 10:59 AM

 Fig. 5.9. A comparison
of fruit and seed
sizes found in dry
forest on Puerto Rico
(Guanica), Isla Santa
Fe in the Galapagos,
and tiny Mona Island
in the West Indies.
The longest dimension
of the fruit or seed of
each plant species was
recorded for each site.

nine on Puerto Rico). These four species on Southwest Pacific islands. While this
are much more abundant on Mona than may be a clue to the steeper species-area
at the Puerto Rican site, suggesting that curve found in this region, it points out
they are able to use most of the fruit and potential problems in trying to general-
seed resource that is subdivided by more ize from one island system to the next.
species in the larger community.14 We will finally understand the structure
Constraints on Avian Diversity

No one has measured available seed of all these communities when we have
sizes on Southwest Pacific islands, but some feeling for the resource base,
stomach content data from Diamond are the dynamics of colonization, and the
revealing.15 He shows the regular exis- mechanisms used by competing species
tence on small islands of fruit pigeons to achieve a place in an island com-
weighing over 800 g (compared to a munity. Until then, we should look at
maximum of 250 g in the West Indies) interisland variation as an opportunity to
that feed primarily on fruit larger than better understand the interplay between
25 mm. Apparently, there is a much species interactions and resource bases
greater range of available resource sizes in different situations.

141

1stPages_A.indd 141 7/22/20 11:00 AM

 Fig. 5.10. The largest member of the fruit-
variety of evidence from the islands sup-
eating guild from the Galapagos Islands
ports some controls to composition and
(front), West Indies (middle), and Southwest
Pacific (back). structure of mainland avifaunas.
In the West Indies, the difficulty
of generalizing patterns for mainland
communities lies in the simplicity of
even the most diverse West Indian
The generality of island patterns island. Virtually all South American
habitats contain many more species
We next ask whether patterns or “rules” than the 60 found on all of Hispaniola
that apply to islands of varying size can or the 30 found together in Hispaniolan
be extended to larger mainland areas. dry forest. Fortunately, a stepping-stone
While the prevalence of the effects of situation exists in the presence of
competition in structuring all island several New World land-bridge islands
communities suggests that some pat- that support species totals from West
terns might exist in larger faunas, it is a Indian levels to the nearly 200 species
chapter 5

giant step from fewer than 100 species of Trinidad. As noted earlier, these land-
on a West Indian island to the nearly bridge communities are composed of
3,000 species in South America. Yet a remnants of larger communities that

142

1stPages_A.indd 142 7/22/20 11:00 AM

 existed when these areas were part of have some correlations with patterns
the mainland, so in many ways they of mainland bird distributions. We can
serve as hybrids between islands and construct regressions of the number
the mainland. Recent work divided the of species within a family against the
species occurring on several of these total number of species for land-bridge
land-bridge islands (Trinidad, Tobago, islands and geopolitical areas of the
Coiba, and five of the Pearl Islands) into mainland.16 To the extent that bird fam-
the same guilds used in the West Indian ilies represent ecological groups, these
surveys noted above. Generally, whole data suggest some structural controls.
families of land-bridge island birds were While this does not explain much about
assigned to a guild to compensate for the structure of mainland communities,
the more complex avifauna on these
islands and the lack of knowledge about Fig. 5.11. Relationship between number of
some species. The results were plotted species in a guild and total land bird species for
as guild membership (number of spe- eight Neotropical land-bridge islands (points)
cies) against the land bird species totals compared to the West Indian regressions for
of each island, as was done with the this same factor, as shown in figure 5.6. Note
West Indies. Amazingly, the West Indian that the gleaning insectivore relationship is
regressions for guild structure did an identical for both locations, while the text
excellent job of predicting the guild explains the differences between flycatcher and
composition of land-bridge islands for frugivore patterns.
all guilds but the nectarivores (fig. 5.11).
Some of the variation in the flycatcher
and frugivore guilds could have been
removed by shifting certain members
of the Tyrannidae (a family composed
mostly of flycatchers but with a few fruit
eaters in the subfamily Elaeninae) into
the frugivore guild.
Comparing species per guild and
area would not provide a similar set of
results, as the land-bridge islands have
different species-area relationships than
the West Indian islands. For example,
Constraints on Avian Diversity

some of the Pearl Islands that contain

20–25 species are much smaller than
Mona Island, which supports 11 land
bird species. To the extent that the
equilibrium number of species within a
guild is the critical factor in structuring
an island fauna, the consistency of guild
composition on this set of highly vari-
able islands is remarkable.
These New World island patterns

143

1stPages_A.indd 143 7/22/20 11:00 AM

 it certainly suggests the continuation of ical patterns by making comparisons
some form of ecological constraint from between different locations. Here we
simple island communities to regions of will look at comparisons made from
the mainland. species lists for the whole world, lists
The diversity of Southwest Pacific made along a tropical to temperate gra-
islands provides a smoother gradient of dient, species found in similar habitats
communities from island to mainland, in different locations of the world, and
particularly since New Guinea is big species composition along a mountain
enough to consider as mainland. An gradient in the Andes. We will also look
examination of taxonomic composition at several detailed studies of structure
on these islands and nearby mainland in single locations. These latter studies
areas shows consistent patterns of are presently of value for the detailed
occurrence;17 it also reinforces some of statistical descriptions they give us of
the differences between New and Old community structure, but only recently
World islands. While this still does not have these techniques been used for
explain how a 400-bird community is geographical comparisons.18 As these
developed on the mainland, it suggests sophisticated techniques are applied to
some pattern in the number and types the appropriate geographical compari-
of species that can coexist in particular sons, community ecology should be able
habitats in different parts of the world. to make great advances in understand-
ing complex mainland avifaunas.
Mainland Evidence of Ecological Before we begin looking at this
Constraints evidence of controls on diversity, we
must look at the types of diversity that
Looking at mainland patterns in the exist. To do this, let us consider some
structure of bird communities is a big of the West Indian islands we looked
step beyond looking at an island, even at earlier. As island size increased,
one the size of New Guinea. South total species increased, but on larger
America, for example, has around 3,000 islands the number of species within
species. While most localities in South a habitat reached a saturation level. To
America may have no more species than understand the composition of the bird
a location in New Guinea, the task of community on a large island, we need
dealing with so many South American to know how species that live together
species and such a large geographic area in different habitats interact and how
is almost overwhelming. If we look at all species composition changes between
the continents, the chore is even greater. habitats. The same would be true for
Despite the complexity of the task, understanding a mainland bird commu-
there are some approaches to the study nity, but on a much larger scale. These
of mainland bird communities that can components of diversity have been given
give us insight into ecological factors names to aid in handling them. Alpha
that affect the structure of these com- diversity refers to the number of species
chapter 5

munities. Many of these approaches living within a habitat or single location.

incorporate what is known as geograph- Gamma diversity is the total number of
ical ecology, that is, looking for ecolog- species living in some designated area.

144

1stPages_A.indd 144 7/22/20 11:00 AM

 Gamma diversity is obviously a function Although this technique was crude,
of alpha diversity (the number of species it provided some interesting insights
in any site) and the change in species into trophic similarities and taxonomic
composition between sites, which is differences between avifaunas. There is
known as beta diversity. While alpha and a great tendency toward trophic similar-
gamma diversity are easy to measure ity in avifaunas despite relatively little
(lists of species are the simplest way), taxonomic similarity. The four regions
beta diversity is harder to measure but that contain tropical habitats are dis-
is a critical concept in understanding tinctly different from the two temperate
the construction of bird communities in regions, with generally little trophic
large areas. variation within members of these two
climatic categories. The amount of tro-
Trophic comparisons of the phic convergence is often pronounced;
world’s avifaunas for example, the Neotropical region
(primarily South America) shares fewer
To the extent that similar habitats in than 20% of its species with other trop-
different areas offer a similar set of ical realms yet has trophic scores very
resources for birds, we might expect that similar to those found in other tropical
evolution would lead to bird commu- locales.
nities with a similar number of species In addition to general trophic
using different types of foods in particu- convergence in regions with climatic
lar ways. In an extensive trophic compar- similarities, this study also suggested a
ison of the world’s birds using the land few cases of distinct variation in trophic
bird species lists for six faunal regions structure. For example, the Australian
(zoogeographic realms), indices of both region is decidedly depauperate in
taxonomic and trophic similarity were ground-dwelling insectivores (which
computed.19 The former indicated varia- may be a historical phenomenon), while
tion in the relative composition of each the Palearctic fauna seems low in nectar
family in the total species pool of each feeders (which may reflect the temperate
region. The latter measure assigned a nature of that climate).
trophic status to all families from seven
food or foraging guilds (birds that eat Latitudinal gradients in species diversity
vertebrates, ground invertebrates, foli-
age invertebrates, aerial invertebrates, Although limited in detail, geographic
Constraints on Avian Diversity

fruit, seeds, or nectar), with each family patterns of variation in gamma diver-
assigned a total trophic value of 1.0, sity can provide insight into structural
which could be divided into fractional constraints in mainland communities.
components. Multiplying species com- The most pronounced gradient of this
position by trophic composition for all type is that associated with latitude. A
families gave a fauna-wide trophic value dedicated bird-watcher in temperate
that could be compared from region to North America can work diligently for
region and could also be standardized years in a county or state without find-
to see whether extreme shifts in trophic ing 300 species. Yet many tropical areas
structure occurred. of a few square kilometers contain over

145

1stPages_A.indd 145 7/22/20 11:00 AM

 500 species. Some of the characteristics 3. The amount of vegetative produc-
of this latitudinal gradient are shown tivity or the predictability (in seasonal
for both alpha and gamma diversity in areas) of such productivity.
figure 5.12. 4. The vegetative complexity of
There have been numerous attempts tropical forests compared with tem-
to explain the causes of this gradient, perate forests, including variation in
focusing on either the ultimate reasons seasonality and size of such resources
why the tropics can hold more species as fruit, flowers, and insects.
or the proximate mechanisms by which
species are added. Ultimate factors While all these factors may play some
examined include the following: role in affecting bird diversity, they are
so interrelated and tropical habitats
1. The amount of time tropical ar- vary so much that we cannot pick any
eas have had to evolve species without of these as the most important cause of
disasters such as glaciers. increased tropical diversity. Certainly the
2. The stability or, in forests with fact that even seasonal habitats in the
seasonal rainfall, the predictability of
tropical climates. Tropical areas are Fig. 5.12. Latitudinal gradients in alpha
often defined as having no frost and (within-habitat) diversity in winter and
greater daily temperature variation summer in North America. The seasonal
than seasonal variation in mean tem- differences reflect the role of migration through
perature. the annual cycle.
chapter 5

146

1stPages_A.indd 146 7/22/20 11:00 AM

 tropics are not exposed to extremely cold round to be fruit specialists. A similar
conditions makes them more benign story can be told for the flower resource
than any temperate habitat; adaptations and nectar-feeding birds. While only one
to dry periods must be easier for birds hummingbird species breeds in all of
than those needed to survive long, exces- eastern North America, tiny Panama has
sively cold periods. over 50 hummingbird species and 10
Proximate causes of this latitudinal other nectar specialists year round.
gradient in species diversity deal with Insects are found all year in the
available resources and the interactions temperate zone, but in winter they may
among species. Inasmuch as some be dormant or in pupal stages and little
measures of these factors can be made, growth in populations occurs. Although
a more precise answer to the diversity some large insects exist, they occur regu-
questions can be gained at this level. As larly only at the end of summer. In con-
might be expected with such a “diverse” trast, tropical insects can grow all year
phenomenon, multiple factors appear to such that large insects are a regularly
be at work. The two major factors seem available resource. This general gradient
to be (1) a closer packing of species on in insect size availability is matched by
resource dimensions, and (2) the avail- a gradient in the sizes of bills of insect-­
ability of “new” resources in the tropics. eating birds (fig. 5.14).
It appears that tropical birds often recog- Numerous other, more specific trop-
nize finer divisions of habitats or habitat ical resources have opened up opportu-
types than do temperate species and nities for specialization by birds. The epi-
thus can pack more tightly along food phytic (“air”) plants that commonly occur
or habitat resource axes. Remember the on the branches of trees are a resource
five coexisting Myrmotherula antbirds of that is largely unavailable in temperate
the tropics separated by foraging height areas. One of these, mistletoe, has a set
as discussed in chapter 4. of specialized species that eats its berries.
The “new” resources available in the Other birds search for insects only in the
tropics are those that are either totally many bromeliads (pineapple-like plants)
unavailable in the temperate zone or found in tropical forests. Swarms of army
so seasonal that few temperate species ants are common in the New World, and
can exist by specializing on them. In many species of birds feed on the insects
other cases, the amount or variety of disturbed by these ants. Certain species
a resource may increase greatly in the (termed “professional ant followers”)
Constraints on Avian Diversity

tropics and allow many species to adapt feed only when they happen to be near a
to it. Dominant among the “new” tropi- swarm, while others visit these swarms
cal resource types are fruits, flowers, and more opportunistically.
large insects. Unlike temperate areas, In some cases, tropical plants and
tropical forests have fresh fruit avail- birds seem to have developed mutu-
able throughout the year (fig. 5.13), so alistic relationships with one another
a wealth of tropical species are adapted through a process called coevolution
to fruit eating. While many temperate (the coupled evolution of two or more
species will eat fruit when it is available, species). A plant attempting to pollinate
only a few can find enough fruit year a distant plant might accomplish this

147

1stPages_A.indd 147 7/22/20 11:00 AM

 Fig. 5.13. Number of fruits and seeds falling disperser; to “pay” for this service, the
into ground traps in a Panamanian rainforest Miconia fruit contains fats and proteins
through the year. Note that all months had such that manakins can survive almost
some fruits and seeds. totally on the fruit and even feed it to
their young. Fruiting seasons of the
by attracting a long-distance pollinator various Miconia species on Trinidad
(such as a hummingbird) by providing are spaced throughout the year, thereby
the bird a good nectar meal at a distinc- ensuring a good supply of manakins.20
tive flower. If the hummingbird feeds, Such specialized adaptations between
gets covered with pollen, and then species rarely occur in temperate areas
travels to a distant flower for another but add significantly to the diversity of
good meal, the plant has succeeded. the tropics.
With time, relationships like this can In making temperate-tropical
result in the specialization of the flower comparisons, we can often see where
to the pollinator and vice versa. Similar tighter packing of both species and new
mutualisms occur between frugivorous resources could be at work. Consider the
birds and plants that want their fruits five tropical kingfisher species we looked
dispersed. Perhaps the classic example at in chapter 4. In the tropics, they live
of such a relationship is between the together and differ in food size and, to a
manakins, a set of New World fruit-eat- lesser extent, in habitat. In North Amer-
ing birds, and the plant genus Miconia. ica north of Mexico, only one breeding
Although able to eat other fruits, certain kingfisher is found, and it is of interme-
manakins feed heavily on the fruit of diate size. Along the Texas-Mexico bor-
chapter 5

Miconia, thereby dispersing its seeds. der, this is replaced by two kingfishers,
The plant gains a competitive advantage one larger and one smaller (fig. 5.15).
over other plants by having its own fruit Farther south, other kingfishers fill the

148

1stPages_A.indd 148 7/22/20 11:01 AM

 various size gaps until the full commu- areas, we occasionally see pairs of spe-
nity of five species is achieved. Certainly, cies that seem to be ecological counter-
a wider range of fish sizes is being eaten parts of one another. In some cases, this
by the diverse tropical set of species, but ecological convergence is matched by
the steps from one to two and from two morphological convergence. Such con-
to five species also seem to involve an vergence has been suggested to be good
element of increased subdivision of the evidence for the existence of ecological
fish resource, which is permitted by the pressures in structuring the characteris-
benign tropical environment. In many tics of both individual bird species and
other cases, a single temperate species is whole communities. Convergence in
replaced by two species at the southern simple communities such as those of
limit of its range. grasslands may not be too surprising,
The addition of different resources considering the relatively limited set
and the development of more diverse of resources available in these habitats
bird communities are common to all and the limited number of ways these
temperate-tropical gradients in the resources can be subdivided. Even then,
world. Although some of the details we need not expect perfectly convergent
may be different in different regions,
all show similar basic patterns in the
Fig. 5.14. Variation in insect size (shaded)
assembly of tropical communities.
in temperate forest, tropical dry forest, and
tropical rainforest and a comparison of
Convergent families and species bill length distribution between temperate
forest and tropical rainforest for the families
When comparing bird communities Tyrannidae, Troglodytidae, Parulidae, and
in similar vegetation types in different Cuculidae.

Constraints on Avian Diversity

149

1stPages_A.indd 149 7/22/20 11:01 AM

 Fig. 5.15. Latitudinal
variation in the number
of New World kingfishers,
with a single species in the
temperate zones (yellow)
and as many as four species
in the Amazon (purple).

150

1stPages_A.indd 150 7/22/20 11:02 AM

 pairs, for there are still several options ries but live in similar environments on
available for subdividing resources, different continents. They are so similar
and we do not know how similar the that early taxonomists considered them
resources really are in different areas. the same species. The New World Black-
Nonetheless, a number of cases of throated Blue Warbler ( ) is nearly iden-
almost perfect convergence between dis- tical to the Old World Blue-and-white
tant and distantly related species exist. Flycatcher (Cyanoptila cyanomelana).
In some of these cases, the convergence Different birds that feed on flowers have
encompasses appearance in addition to converged in structure, as have Old and
ecological factors. A classic case of con- New World families that specialize on
vergence at the species level involves the stinging insects. Both Old World and
North American meadowlarks (Sturnella, New World rainforests have many long-
family Icteridae) and the African long- legged, short-tailed forest floor residents
claws (Macronyx, family Motacillidae; known as pittas. Although shaped
fig. 5.16). These nearly identical birds the same way, they share no common
have totally different evolutionary histo-

Constraints on Avian Diversity

Fig. 5.16. Examples of

convergence in appearance
between distantly related
bird species.

151

1stPages_A.indd 151 7/22/20 11:02 AM

 ancestors but evolved their structure for mountain range that lacked many of the
life on the rainforest floor. While these normal high-elevation species.
two groups appear to have converged Over 600 species were recorded
ecologically, their mating systems may along the altitudinal gradient of the
be very different, as the Old World pittas Andean study site. Terborgh attempted
are brilliantly colored, while those of the to evaluate factors that controlled each
New World tend to be fairly cryptic and species’ distribution on the gradient
dull. by assigning each range limit to one of
Although the evolution of identical three possible categories. If a species’
species in separate regions is interest- distribution stopped but it was immedi-
ing, by itself it is of limited value in ately replaced by an ecologically similar
understanding the role of ecological species, the distribution was classified as
pressures in structuring avifaunas. With being limited by competition in the stan-
nearly 10,000 species of birds in the dard form of competitive exclusion. If a
world, we would expect some to resem- species’ distribution stopped at a change
ble one another by chance. Only with in vegetation type (an ecotone), it was
detailed information on the resources said to be limited by some habitat char-
available and the ecological and evo- acteristic associated with that ecotone.
lutionary pressures at work can we be The remaining species that dropped out
sure that these equivalent species arose at various points on the gradient but
from the effects of similar pressures in were not replaced by similar species had
different parts of the world. The fact that to be thrown into a catchall “gradient”
a few have been examined and appear to category, assuming that some property
fulfill these requirements is appealing, of vegetation, resources, or competitive
but further work is needed. interaction had led to the species’ exclu-
sion. With the distributions from just
Competition in an Andean bird one mountainside, Terborgh was limited
community to these three possibilities. He found
that one-third of the species were lim-
We have been moving along a gradient ited by obvious competitive interactions
of approach, from studies on a global and one-sixth by apparent ecotones.
scale to more regional comparisons. About half the species were left for the
Here we want to examine a classic study gradient category.
confined to two slopes of the Andes of The upper reaches of the isolated
Peru, conducted by John Terborgh.21 mountain in the Sierra de Sira looked
Over several years, he and his col- like a normal Andean mountain in
leagues did extensive surveying along vegetation but lacked many (82%) of the
these slopes from the lowlands to their normal high-elevation birds. Assuming
summits. Both slopes shared similar that this vegetation provided a normal
climates and vegetation types, but one distribution of bird foods, we can make
was a part of the main chain of Andean several predictions about what Terborgh
chapter 5

mountains and had a high diversity of should have found. Lowland species
species from top to bottom. The sec- whose distribution in the main Andes
ond study area was part of an isolated was limited altitudinally by competi-

152

1stPages_A.indd 152 7/22/20 11:02 AM

 tion with a similar species should have Single-location studies
expanded their altitudinal range when
that competitor was absent in the Sira. Using geographical comparisons to
Such an observation would reinforce study communities is about as close
the importance of competitive exclusion as we can get in field studies to doing
in limiting distributions. If a species experiments. By comparing two islands
assigned to an ecotonal or gradient or two similar habitats in different areas,
limitation was in fact limited by some we can often gain insights that could
vegetative characteristic, it should con- not be gathered with a more intensive
tinue to be so limited in the Sira. If it look at a single site. Obviously, not all
was limited by a diffuse assemblage of ecological questions can be answered
competitors, we might predict that with by this approach. In particular, as we
fewer high-elevation avian competitors discover the more superficial patterns
in the Sira, it should expand its range in the structure of bird communities,
altitudinally. In other words, we could we need to make more detailed obser-
predict that the existence of fewer spe- vations of these communities to answer
cies to divide an equivalent area and set questions about annual variation in
of resources should result in the altitudi- structure, resource supply, the effects of
nal expansion of many of those species. unusual climatic events, and so forth.
The data supported these predic- The problem that arises in accomplish-
tions, with most species expanding as ing all of this is related to allocation of
expected when some form of competi- time and money; very detailed examina-
tion (direct, or what is known as diffuse tions of community structure within a
competition) has been a limiting factor. site tend to take all the time and money
In the final analysis, Terborgh felt that a researcher can gather. If researchers
71% of the species distributions on the want to study two or three sites, they
Andean mountain were limited by some must often reduce the intensity at each.
form of competitive interaction, with the As time goes on, it is hoped that more
remaining species limited by vegetation intensive approaches within sites can be
or resource changes associated with the incorporated with geographic compari-
altitudinal gradient. sons, but the amount of work involved
Other aspects of community struc- will always be a problem.
ture were also examined in this study. Perhaps the epitome of a detailed,
Many changes in foraging guild struc- long-term study at a single site is the
Constraints on Avian Diversity

ture occurred, often because of resource work being done by R. T. Holmes and
changes as the climate and vegetation colleagues at Dartmouth in the Hubbard
changed going up the mountain. While Brook watershed of New Hampshire.22
much remains to be understood about They have done extensive year-long sur-
all the factors at work in structuring veying and banding of birds to monitor
these communities, this study provides populations, along with detailed stud-
exciting evidence that such factors have ies on food supplies, nesting success,
some effects, and that with the proper homing, and other behaviors. The use
approaches they can be understood in a of modern statistical techniques such
complex avifauna. as multivariate and cluster analyses has

153

1stPages_A.indd 153 7/22/20 11:02 AM

 allowed them to describe a variety of we want to believe that bird commu-
structural patterns within this commu- nities are highly structured through
nity. They have made some interesting competitive interactions or the result of
observations as to which community single-species interactions solely with
characteristics change with either very their own environments. Although this
high or very low food supplies, obser- author is biased in favor of a strong role
vations that further our understanding of interspecific interactions in struc-
of avian community dynamics. Some of turing bird communities, this does not
the most detailed work ever done on the exclude the effects of history or other
cues that species use in habitat selection factors. In many cases, situations where
and foraging behavior has also been part apparent “rules” of structure are bro-
of this project.23 ken are often revealing because of the
Although the first years of the way they may support the existence of
Holmes study were confined to an the “rules” in other situations. Avian
incredibly detailed inventory at a single community ecology has a multitude of
location, they recently compared this questions to answer: Is the Palearctic
site with one in Australia.24 The future avifauna lacking in nectarivores because
of avian community ecology undoubt- of a lack of flowers, or because of ocean
edly involves studies that incorporate and mountain barriers that have kept
detailed work at single locations, includ- tropical colonists away? To what extent
ing the appropriate statistical techniques is the lower diversity of ground-dwelling
that allow us to deal with complex sets insectivores in Australia a result of the
of species within properly conceived high diversities of insectivorous lizards
geographical comparisons that allow the there? Do fish-eating owls occur only in
maximum gain for the effort involved. the Old World because the New World
has fish-eating bats? Answering these
Final Comments: What Is Structure? and similar questions will require mixed
approaches ranging from detailed stud-
As we mentioned earlier, our examples ies to geographical comparisons. With
of studies searching for patterns of the answers will come a greater under-
community structure show some of the standing of how the diversity of birds
ecological factors that affect bird com- has evolved.
munities. These factors exist whether
chapter 5

154

1stPages_A.indd 154 7/22/20 11:03 AM

 C HA PT E R 6

Systematics
and Taxonomy
Classifying Birds

I
n the previous chapters we have (through the systematic techniques we
outlined some of the genetic, will discuss later), taxonomy provides a
behavioral, and ecological processes set of names that describe these rela-
that may have produced the nearly tionships. The structural format in use
10,000 existing species of birds we see for taxonomy today is still basically the
on earth today. Classifying these 10,000 one developed by Linnaeus in 1758.
species in some manner that allows us The basic building block of this system
to understand the evolutionary (phylo- is the species, described by a Greek or
genetic) relationships among different Latin binomial. The other categories
forms is the province of systematics are hierarchical in nature, using names
and taxonomy. The goal of avian sys- to denote clusters of species or higher
tematics is to understand the kinds and groups that are more closely related than
diversity of birds and the relationships other such clusters. We have already dis-
among them such that these taxa can cussed how species can be broken into
be arranged into a hierarchical scheme groups called subspecies, usually based
based on their evolutionary relation- on geographical variation in morphol-
ships. Avian taxonomy deals with the ogy; species that are considered more
theory and practice of naming the cate- related to one another than to other spe-
gories that result. Although some people cies are put in the same genus. Related
use the terms “systematics” and “taxon- genera are grouped into families, and
omy” almost interchangeably, they refer related families are grouped into orders.
to separate, though complementary, Thus, the basic division of the class Aves
sciences. In this chapter we will examine uses order, family, genus, and species.
how the goals of taxonomy and sys- To denote more detailed relation-
tematics may be achieved, ending with a ships among groups, taxonomists also
classification of the world’s birds. recognize a variety of in-between classi-
fications, usually denoted by the prefix
Taxonomic Categories “sub” if it divides a group at a slightly
lower classification, or by the prefix
Once a decision has been made about “super” if it connects groups at a slightly
the proper phylogenetic relationships higher level. Thus, an order with several
of the groups of organisms under study families may be divided into suborders,

155

1stPages_A.indd 155 7/22/20 11:03 AM

 or these families may be connected as tered by the International Commission
superfamilies. Many times it may seem on Zoological Nomenclature.
that these changes accomplish the same Although the structural rules of
result, but one or the other is generally the classification scheme have been
more appropriate to a particular set of fairly consistent for over 200 years, the
circumstances. Adding these categories philosophies and methodologies of the
leaves a potential taxonomic hierarchy systematics that affect this taxonomy
of class-subclass-superorder-order-sub- have changed dramatically over that
order-superfamily-family-subfami- period. We must remember that Lin-
ly-tribe-supergenus-genus-subgenus-su- naeus developed this system over 100
perspecies-species-subspecies (see table years before the theory of evolution by
6.1 for an example). natural selection had been developed by
The scientific nomenclature used Charles Darwin and Alfred Russel Wal-
for each of these levels follows specific lace. At that time, creationism was the
rules. We have already seen the Latin dominant theory for the origin of spe-
and Greek roots for species, subspecies, cies, and species were considered fixed
and genus. Family names end in “idae,” entities that could not change. Although
subfamilies in “inae,” tribes in “ini,” and people recognized that some species
superfamilies in “oidea.” Orders always groups were more similar than other
end in “iformes,” but suborder names groups, there was not a good under-
are less regular. The rules that apply for standing of how species were made or
the use of these categories are adminis- how they might be related. The result

Table 6.1
Taxonomic designations and general traits for the largest
race of Canada Goose
taxonomic designation traits of designation
Kingdom Animalia Separates group from plants and unicellular animals
Phylum Chordata Group of animals with hollow nerve cords, gill slits,
etc.
Subphylum Vertebrata Those chordates with backbones
Class Aves Class with feathers and traits covered in chapter 1
Superorder Neognathae Typical birds with “modern” mouthparts
Order Anseriformes Order of waterfowl with webbed feat
Suborder Anseres Typical waterfowl, excludes screamers from the order
Family Anatidae Family of typical ducks, geese, and swans
Subfamily Anserinae Subfamily of geese and swans
Tribe Anserini Tribe of largely terrestrial geese
Genus Branta Group of “brent” geese
Species canadensis Canada Goose of North America
chapter 6

Subspecies maxima The largest race of this species, found in the interior
of North America

156

1stPages_A.indd 156 7/22/20 11:03 AM

 was that early classification schemes larities of species or groups and assign
were basically descriptive, focusing on them to the same taxa. With perfect
morphological traits and developing knowledge of phylogenetic relationships,
taxonomic classifications that grouped the taxonomic systems of lumpers and
species by morphological similarity. This splitters should place all species in the
trend was accentuated because most of same hierarchical position relative to
these studies were done on stuffed birds one another, but the actual taxonomic
in museums; in most cases, information categories could still vary.
on ecology, internal anatomy, and behav-
ior was unavailable. Given this situation, The Development of
it is not surprising that morphologically Modern Systematics
similar but unrelated forms were often
put in similar taxonomic groups, while The goal of all systematists is to develop
in other cases the male and female of a hierarchical scheme that arranges the
particularly dimorphic species were taxa under study according to phyloge-
classified as separate species. With the netic relationships. In an ideal system
development of the theory of evolution, with complete knowledge of avian
greater understanding of genetics and history, the final systematic scheme for
inheritance, and the development of the birds would start with the original bird
biological species concept, the balance and show all the various species that
has changed from using morphological have evolved from it. This would allow
traits alone to using a variety of biolog- us to trace the relationships of all exist-
ical characteristics to discover relation- ing species exactly. Because our knowl-
ships among species. In recent years, edge of avian paleontology is so lim-
the development of molecular biology ited, systematists must generally try to
has totally transformed how most people determine these relationships by looking
do systematics. It is not surprising that at the characteristics of present-day birds
the ability to compare species through while considering factors that could have
molecular biology has also changed how affected speciation patterns in the past.
most taxonomic decisions are made. The basic evolutionary unit is a
Despite the tight interaction population of a species, and much of our
between taxonomy and systematics, they effort attempts to determine relation-
are independent endeavors. Even if all ships both within and among species.
the phylogenetic relationships among This is sometimes a major problem,
the birds of the world were determined, because as we noted in chapter 4, spe-
Systematics and Taxonomy

this would not result in a single taxo- cies are sometimes difficult to describe
nomic scheme. Taxonomists will always accurately. If the basic units of a hierar-
disagree about the amount of difference chical system are improperly identified,
necessary to separate taxonomic cate- then the whole system develops prob-
gories. People who focus on the differ- lems. In many cases, though, species
ences between species or groups and and even subspecific variation can be
tend to put them in separate taxa are accurately described and serve as a solid
known as “splitters.” “Lumpers,” on the basis for systematic comparisons.
other hand, tend to focus on the simi- Even when species traits are dis-

157

1stPages_A.indd 157 7/22/20 11:03 AM

 tinctly determinable, difficulty arises in from the Galapagos were quite separate
trying to determine the relationships from any of the finches found elsewhere
that result in higher taxonomic catego- in the world, although the original col-
ries such as genus and family. There onist species had to come from some-
are no biological rules (such as lack of where. As we will see in more detail
interbreeding) that define the genus or below, recent studies are attempting to
family. Rather, systematists examine look directly at genetic traits rather than
large numbers of species and try to find phenotypic traits to minimize the effects
clusters of species sharing particular of morphological convergence in deter-
biological traits, including living in the mining relationships.
same region. These clusters are then
defined as the various possible higher Traditional approaches to systematics
categories. Some problems arise simply
from adhering to the assortment of Lin- Several schools of thought have devel-
naean categories, as there is no biologi- oped regarding the procedures that
cal reason why the relationships of sets should be used when studying system-
of species should always match such a atic relationships among species. The
system. approach that dominated systematics
Determining these relationships until fairly recently (and is thus termed
among a great many species that have the traditional or eclectic approach)
been evolutionarily separated for mil- examined evidence from a variety of spe-
lions of years is not an easy task. Con- cies to try to determine relationships by
founding efforts to trace phylogenetic the similarities and differences among
histories are patterns of convergence, traits of these species. Clusters of
as shown in chapter 5, or of radiation, species with distinctive traits would be
as shown in island birds in chapter 4. described and evolutionary relationships
For example, early taxonomists placed would be suggested to fit these clusters
members of the Hawaiian honeycreeper in an appropriate taxonomic hierarchy.
group in several families based on The traditional approach has a vari-
bill structure and general appearance. ety of weaknesses, depending in large
Obviously, we must be careful about part on the type or number of traits that
choosing the traits to compare between are examined when looking for rela-
species and attempting to reconstruct tionships. In some cases, systematists
phylogenetic relationships. Traits such that specialized on a particular bone or
as bills or plumage that seem fairly flex- muscle system constructed whole phy-
ible are often not good for phylogenetic logenies from this material. Although
studies, while traits such as muscles and this sometimes worked, in other cases
bones are often quite conservative and they classified related groups at different
may show relationships even if the over- levels because they focused too much
all body shape of the bird is changing. on small differences in structure. Earlier
Knowledge of where birds came from we mentioned the controversy over the
chapter 6

and how much they could move around classification of the large grazing birds
also had to be incorporated into these of the world (ostriches and such). These
studies; obviously, Darwin’s finches have been put in the avian superor-

158

1stPages_A.indd 158 7/22/20 11:03 AM

 der Paleognathae with the primarily stapes. The primitive structure of the
terrestrial tinamous because these stapes is circular, with variable amounts
groups all share what is considered a of support and a long stalk (fig. 6.1). The
primitive structure of the bony parts of stapes in hoopoes and woodhoopoes has
the jaw and mouth (paleo means “old” a very different structure, which sug-
and gnathae refers to the mouth and gests it is a derived trait. The fact that
jaw). All other orders are considered these two species share such a similar
Neognathae (“new mouths”) and have bone structure suggests that they are
differently structured jaws. The assump- more closely related to one another than
tion involved with this classification is to any other groups.2
that jaw structure is a trait that does not Obviously, the more traits that are
change rapidly, and therefore birds with compared between groups of birds, the
similar jaw structure must have similar better the classification scheme should
evolutionary histories. This assump- be. Even with multiple traits, though,
tion has been questioned by the recent traditional systematic approaches run
discovery of the bones of a flightless
ibis in Hawaii; although much evidence
confirms that this bird was an ibis, it
appeared to be in the process of develop- Fig. 6.1. Variation in the structure of the
ing a paleognathous jaw.1 This suggests stapes, an inner ear bone. Primitive forms of
that a paleognathous jaw may have the stapes (left) are round, with varying details
of structure and a long, thin columella. In
evolved more than once, so it must be
hoopoes and woodhoopoes (center), the stapes
used with caution when trying to cluster
is anvil shaped. This derived structure suggests
species. that these two groups are closely related, but
Another trait that has often been not closely related to groups with the primitive
used involves the middle ear bone, or stapes (Feduccia 1977).

Systematics and Taxonomy

159

1stPages_A.indd 159 7/22/20 11:04 AM

 into problems with subjective judg- should most approximate a phylogenetic
ments about which traits to use, which classification when a large number of
are the most meaningful, how much measured traits is included. With just
difference is necessary to constitute a few characteristics of bill or body size
different clusters, and so forth. Although included, the Hawaiian honeycreepers
the traditional approach has been might well be separated by larger gaps.
almost completely replaced by newer Presumably, the inclusion of many
approaches and new types of evidence, internal measures of traits that vary
in many cases these new approaches conservatively would show the phylo-
confirm that traditional methods often genetic similarity within the Hawaiian
worked well in defining smaller groups honeycreepers despite the differences in
such as families and genera. some external characters. The possibility
that convergent but unrelated forms will
Numerical approach to systematics be classified together is still a weak-
ness of using numerical techniques in
An attempt to remedy some of the taxonomy, but this approach had value
weaknesses of traditional approaches in advancing systematics, particularly by
appeared in what is now known as the development of computer programs
numerical or phenetic taxonomy. This that could handle large sets of compara-
technique attempted to classify organ- ble data.
isms by measuring vast numbers of
traits among a group of species and then Cladistic approach to systematics
constructing hierarchies using statistical
procedures that cluster similar groups The most modern approach to classi-
of species within those measured. This fying organisms is known as cladis-
approach attempts to remedy the arbi- tics.4 This approach uses many of the
trariness of traditional approaches both same types of evidence as traditional or
by using large numbers of traits to com- numerical approaches, but it attempts
pare species and by using mathematical to compare species groups and develop
differences between clusters to provide hierarchies in a more rigorously scien-
quantitative guidelines of similarity. For tific fashion than traditional approaches.
example, the suborder Lari (gulls, terns, Cladistics attempts to determine
and relatives) was examined in this way whether a particular trait is primitive
using measures of 51 skeletal and 72 (found in a number of forms so that it
external traits;3 such approaches were appears to be ancestral) or derived (a
not possible prior to the development of trait that is shared by a group of species,
computers that could handle all the data appears to have developed within the
generated by a comparison of 123 traits group, and therefore helps distinguish
in nearly 100 species. that group from others). Obviously,
Although often used for systematic these categories are relative, as feathers
classifications, phenetic techniques are derived when comparing vertebrates
chapter 6

primarily provide a method of measur- but may be considered primitive within

ing overall similarity among a group birds, depending on which avian origin
of forms. A phenetic classification is favored.

160

1stPages_A.indd 160 7/22/20 11:04 AM

 The primitive or derived status of a groups. Biases that seem to appear from
trait is determined by comparing that selecting characteristics to compare (as
trait between the group under study in the traditional approach) are neu-
(termed the ingroup) and one or more tralized by the ingroup-outgroup com-
selected groups of other species (termed parison technique. Because cladistics
outgroups). If a trait is shared between traces lineages over history, it can more
the ingroup and outgroup(s), it is con- comfortably handle changes within a
sidered primitive for the ingroup and is species that occur over time than can the
not useful for determining phylogenetic other techniques.
relationships within the ingroup. If the Some form of cladistic approach
trait is found only in the ingroup, it is dominates modern studies of avian sys-
considered a derived trait at the level tematics, particularly when systematists
of the ingroup. These comparisons are are looking at higher taxonomic catego-
done as hypothesis testing following the ries (genus or family). Although some
standard scientific method; they can be recent cladistic analyses have shown that
done with a series of different outgroups traditional approaches gave mislead-
to determine whether the trait is derived ing results, in many cases the cladistic
within the ingroup. Using this method approach has only reinforced taxonomic
repeatedly for a series of characteristics categorizations done by more traditional
and a variety of ingroups should result methods. This is not to say that fur-
in a classification scheme that clusters ther work will not change many of the
those species sharing particular derived taxonomic groupings we use currently;
traits as most closely related. cladistic analyses and the advances in
Cladistics focuses on splits within biochemical approaches to determining
phylogenetic lineages throughout its relationships (see below) may greatly
analyses. This results in sister groups alter our understanding of phylogenetic
that are termed monophyletic (a taxon relationships, particularly at higher
containing all the descendants, and only taxonomic levels. Yet thorough studies
the descendants, of a common ances- detailing similarities and differences
tor), in contrast to polyphyletic (a taxon among forms should not be discounted
composed of two or more independent solely because of the use of traditional
lineages). Cladistics gets its name methods.
because these monophyletic groups are
known as clades. In addition to a rigor- Evidence Used in Systematic Studies
ous hypothesis-testing format, cladistics
Systematics and Taxonomy

has firm rules that require sister lin- Any avian characteristic that has a
eages to be of the same taxonomic rank. genetic basis can be of use in systematic
The cladistic approach combines studies. Obviously, traits that show great
some of the strengths of both traditional phenotypic (environmental) variation
and numerical approaches. Much of among individuals are not as good for
the detailed descriptive work done with determining evolutionary relationships.
these older approaches can be subjected As we noted above, the value of a partic-
to cladistic analyses if enough informa- ular trait in evolutionary studies varies
tion exists for both ingroups and out- with its degree of flexibility. Highly

161

1stPages_A.indd 161 7/22/20 11:04 AM

 plastic traits (such as bill type) may be been useful, but rarely are these traits
of little use because they vary too readily of value in determining relationships at
to show relationships, but highly non- higher taxonomic levels.
variable traits (such as the avian heart)
are also of limited value because they Morphological and physiological traits
do not show enough variation. Different
use may be made of traits when trying Morphological traits have long held
to determine relationships at different great importance in systematic stud-
taxonomic levels; factors such as behav- ies, partly because of their generally
ior and ecology may help distinguish conservative nature and partly because
relationships among groups of similar systematic studies began in muse-
species, but they are rarely of help in ums, where study skins and skeletons
comparing families or orders. A vast were readily available. A great variety
array of traits have been of use to avian of morphological features have been
systematists; the survey here can pro- useful in systematic studies at many
vide only a brief introduction to some of levels. Everything from plumage color or
these and how they are used. other external features to the structure
of chromosomes may be of systematic
Behavioral and ecological characteristics use. Physiological traits such as molting
or reproductive patterns may also be
To the extent that behavioral traits such valuable. As noted before, the worth of
as song, courtship, nest building, or hab- each trait varies with the extent to which
itat selection are genetically determined it is genetically determined and the flex-
and relatively conservative, they may ibility of evolution within the trait. For
be of use in determining relationships. example, early workers suggested that
These traits are most often useful when the structure of the bony covering of the
comparing small sets of similar species; legs (the scutes) was a conservative trait
a comparison of displays among three that suggested relationships; later work
species of marsh blackbirds makes showed this to be of little taxonomic
it clear that Red-winged Blackbirds value.
(Agelaius phoeniceus) are more closely We have mentioned several mor-
related to Tricolored Blackbirds (Agelaius phological traits that have been used for
tricolor) than either of those species is studying relationships (e.g., paleogna-
related to Yellow-headed Blackbirds thous palate, skeletal measurements,
(Xanthocephalus xanthocephalus).5 Song tubular tongue). Among other morpho-
is often an important part of mate attrac- logical traits that have had great impor-
tion among similar-looking species such tance in recent systematic work are the
as flycatchers; in these cases, similarities detailed anatomy of the syrinx, the struc-
in song patterns among species aid the ture of the inner ear, and the structure
determination of phylogenetic patterns. of the hind limb.6 These sets of muscles,
Traits of nest building (materials or tendons, and cartilage appear to show
chapter 6

structure), scratching (over or under the enough variation that they are helpful in
wing), and other behaviors have also delineating relationships among closely
related groups, yet they are not so vari-

162

1stPages_A.indd 162 7/22/20 11:04 AM

 able that they do not provide informa- population variation. In the relatively
tion on relatedness among higher taxa. short period of 60 years, we have gone
Syringeal structure has been particularly from measuring general gene character-
important in systematic studies of the istics or the traits of some gene prod-
order Passeriformes, the perching birds. ucts to being able to describe the exact
The great variation in songs within this genetic structure of the genome. With
group is apparently related to structural these advances, we can now compare the
variations, which are of great use in exact genetic characteristics of organ-
determining relationships. isms throughout the genome. Working
Despite the apparent success of on the assumption that the variation
studies of syringeal or appendicular seen in nature is reflected in DNA, we
anatomy, there is nevertheless the pos- now compare the whole genomes of
sibility of convergence in structure that birds when attempting to understand
could obscure relationships. Yet studies avian systematics. Before we talk about
of morphological patterns will continue where we are today, let’s summarize the
to be important in explaining relation- steps we went through to get here and
ships among certain groups of species. what it means to our understanding of
avian systematics.
Molecular biology and
modern avian systematics Protein electrophoresis

All the traits of birds that were used for Protein electrophoresis is a technique
systematic studies in the past are the that allows a measure of actual gene
products of natural selection acting on products, mostly types of proteins. As
the genetic variation of a population these proteins are the primary product
through sexual reproduction. Humans of gene action, directly translated from
have been selectively breeding organ- sequences of nucleotide base pairs,
isms for thousands of years, but it is this was felt to be very close to studying
only in the past 100 years or so that we actual genetic traits themselves. Many
have started to understand the details of proteins have electrical charges, which
the reproductive process and how varia- are reflected in differences in migration
tion is passed through generations. This rates when tissue extracts are placed in
early work still focused mostly on gene an electric field. With the potential for
products and how traits were passed several forms of a protein at each locus
through populations as we developed (gene) and many possible loci, a great
Systematics and Taxonomy

the biological species concept. many genes could be examined.

Since the discovery of the detailed Electrophoretic variability was useful
structure of DNA in 1953 and the way in a variety of studies. At the individual
that the double helix works to carry level, it was used for paternity or mater-
genetic variation during reproduction, nity testing within different mating
we have made tremendous strides in systems (see chapter 12). Systematists
our ability to both understand how the used electrophoresis at nearly all levels,
system works and measure the details of from examining within-species variation
the DNA involved in reproduction and to searching for patterns of relationships

163

1stPages_A.indd 163 7/22/20 11:04 AM

 among orders. To do this, it was gener- form of skins or skulls while wanting
ally assumed that species that are more to understand relationships through
closely related should be more similar genetic information. All of this changed
in the proteins produced than more dis- with the discovery of the structure of
tantly related forms. Comparing protein DNA and our increased ability to study
traits among a group of species of vary- DNA structure over time.
ing relatedness could result in clusters DNA is the genetic structure that
that could then be ranked taxonomi- changes with natural selection over
cally.7 Such data can also be analyzed in time, so the better systematists can
a cladistic manner, using shared derived measure DNA structure and compare
alleles as traits. If we assume some con- it between individuals, the better they
stant rate of change in the frequency of can understand relationships between
these proteins, we can then estimate the those individuals at the genetic level
age of various species or species groups. with no concern for convergence, indi-
Electrophoretic studies of avian sys- vidual variability, or the other problems
tematics advanced rapidly in the 1970s associated with looking at phenotypes.
and 1980s, partly with advances in the Although the molecular structure of
technology associated with analyzing DNA was discovered in 1953, constraints
proteins and partly from new knowledge on our ability to measure the details of
about how to gather the proper samples. the double helix limited work for many
Some early studies using the proteins years. In the 1970s, Charles Sibley and
from blood found relatively little vari- Jon Ahlquist (1983) started pioneering
ability with which to work; it was found work using the total DNA pool of many
that using other tissues, such as muscle, bird species and measuring relation-
liver, heart, kidney, and feather pulp, ships among major groups of birds
rather than just blood, provided a much through DNA hybridization, which we
greater variety of loci to examine. With describe in more detail below. It was not
the development of molecular tech- until the 1980s that molecular biolo-
niques since the 1980s (some of which gists became proficient at studying the
involve an electrophoretic step or two), details of this genetic structure in a way
these old-fashioned electrophoretic that was fairly easy and repeatable, such
methods pretty much disappeared. that a variety of new genetic techniques
were developed, all of which advanced
Molecular approaches to systematics avian systematics. Now, researchers have
measured the whole genome of some
We all know that adaptations are the species. Dozens of genetics labs exist
result of changes in gene frequencies where we can find matching regions of
through the effects of natural selection the DNA in different bird species and
on interbreeding animals, but there is measure them in terms of the sequences
always the problem of natural selection of base pairs at specific sites; where once
working on phenotypes, while evolution we were lucky to measure a small hand-
chapter 6

involves genetic change. Systematists ful of base pairs, now we can measure
deal with this problem in their own tens of thousands at a time.
way when looking at phenotypes in the Obviously, our knowledge of pat-

164

1stPages_A.indd 164 7/22/20 11:04 AM

 terns in the structure of DNA has caused when heated and homologous pairs
an explosion in studies of avian phylog- will still re-form at the appropriate
eny. Before we talk about some of the temperature. In many cases, however,
problems associated with this explosion, these homologous pairs may be hybrids,
let’s look at some examples of the use composed of one strand from each of
of molecular biology in avian systemat- the two species. If the hybrid DNA is
ics, going from an early, classic study to then exposed to a thermal gradient, it,
more modern methodologies that work too, will break apart. The rate at which
at various taxonomic levels. Systematic the hybrids break down is related to the
work that attempts to measure rela- similarity of base pairs in the strands
tionships at the family or order level making up the hybrid. If most of the
requires different molecular approaches base pairs are homologous on the two
than studies attempting to determine strands, firm bonding occurs and the
whether two allopatric populations are hybrid breaks down at close to the rate
of the same species. we would expect for the “native” DNA
DNA hybridization. Charles Sibley was helices from single species. If there are
an avian systematist who was among the many mismatched pairs, lower tempera-
first to use electrophoretic techniques. tures can break the strands apart.
Before we developed a better under- Curves can be constructed that
standing of the structure of DNA and measure these rates of dissociation in
how to study it, he had the idea to use various species-pair combinations. It
a relatively primitive DNA technique to appears that a drop of 1°C in the dissoci-
attempt to measure phylogenetic pat- ation point is equivalent to an increase of
terns of birds at the order and family about 1% in the number of mismatched
level. pairs. At one point it was suggested that
The technique Sibley chose to use, the single-point mutations that cause the
known as DNA-DNA hybridization, changes in these DNA sequences occur
took advantage of the fact that the DNA at a uniform rate through evolutionary
molecule is a double helix with match- time, so that the differences in DNA
ing base sequences. If this molecule is sequences between two species might
heated to 100°C, the two component also give a measure of the time since the
strands separate because the heat breaks species separated. Later work has sug-
the bonds that hold them together. As gested that this is not the case.8
the solution containing these strands Sibley and his students and col-
cools, the helix re-forms. If this solution leagues ran thousands of these com-
Systematics and Taxonomy

is maintained at a specific temperature parisons of “hybrid” DNA, covering as

(usually around 60°C), only strands that many families of birds of the world as
are complementary (termed homolo- possible.9 By comparing the rates of dis-
gous) will re-form, because only these sociation between forms, he could find
will have enough similarity in match- groups that clustered together because
ing pairs to generate enough bonding of similar DNA structure and some that
strength to overcome the effects of heat. were very different from one another.
If we combine the DNA of two dif- With his taxonomist colleague Burt
ferent species, the strands will separate Monroe, he constructed a new taxonomy

165

1stPages_A.indd 165 7/22/20 11:04 AM

 of birds of the world at the order and to appear more and more primitive,
family level, something that was called even though it was a comparison of the
“the tapestry.”10 In most cases, clusters whole genome of particular bird groups.
corresponded to what had previously Only recently, though, has anyone
been considered related groups, which is attempted to measure relationships at as
perhaps not too surprising. But the rela- broad a level as Sibley and his colleagues
tionships among clusters allowed Sibley did over three decades ago. Before we
and Monroe to combine different levels look at that study, let’s look at the devel-
of taxonomy into orders or families. opment of approaches used by most
For example, up to that point, nearly all systematists over the past 30 years that
orders were categorized by very conser- deal with relationships at the species or
vative morphological traits such as the genus level.
type of webbed foot, the existence of a Molecular biology at lower taxonomic
“tube nose,” and so forth. Relationships levels. As molecular biologists developed
among these orders were not under- the ability to define selected parts of
stood at all; rather, most systematists DNA and then determine the sequence
assumed that aquatic birds were more of DNA bases on those parts, they
closely related to one another than to immediately started to use these meth-
terrestrial birds, but little was known ods to answer questions about species
beyond that. relationships at various levels. Even
By appearing to have a measure of when only a few hundred sequences
similarity among orders at the DNA could be determined, valuable insight
level, Sibley and his colleagues had an into relationships could be gained.
independent measure of relatedness At this level, systematists needed
both within orders and among different to compare sequence variability in a
orders. This new tapestry totally changed variety of individuals of the various
the membership in some orders; it populations under study, because these
seemed that about half the world’s birds measures included the genetic variation
ended up belonging to the Ciconii- that occurred among the individuals
formes (originally the storks), including of a population. Thus, if we wanted to
loons, grebes, petrels, pelicans, raptors, determine whether a group of popula-
and shorebirds (fig. 6.2). On the other tions comprised one or more species,
hand, the order Coraciiformes (rollers) we would want to examine the various
was split into four small orders. clusters that might or might not occur
Sibley was applauded for the breadth among populations and then decide
of his study, but subsequent attempts what the differences among populations
to test many of his taxonomic changes (if they occurred) meant. Decisions
resulted in varying degrees of success. about whether the differences were
Some studies supported the tapestry, but enough to signify species-level distinc-
many did not. A few studies used this tions could then be made. As these sorts
methodology within the family level with of studies accumulated, certain quantita-
chapter 6

good results. Over time, as the method- tive levels of genetic differences among
ology of molecular biology became more populations seemed to be correlated
sophisticated, DNA hybridization came with real taxonomic differences among

166

1stPages_A.indd 166 7/22/20 11:04 AM

 Systematics and Taxonomy

Fig. 6.2. Difference between the orders of birds populations, such that “rules” seemed
under conventional systems (left) and under to develop about how much difference it
the Sibley-Ahlquist system (right) of DNA took to be a species or for species to be
hybridization. Note how many orders were in different genera.
combined into the Ciconiiformes under the In many cases, these molecular data
Sibley-Ahlquist system (Sibley and Ahlquist tested fairly obvious hypotheses about
1983).
species relationships, often falling back

167

1stPages_A.indd 167 7/22/20 11:04 AM

 on situations where species determi- and a few other members of the family
nation was questionable or the genetic as outgroups. Surprisingly, this study
relationships among seemingly closely suggested that the Indigo and Lazuli
related sets of species were unknown. Buntings were not closely related, while
For example, a study of species limits in fact the Blue Grosbeak and Lazuli
in the yellow-breasted meadowlarks Bunting were sister species (fig. 6.3
(Sturnella), which are common in North shows the phylogenetic tree with data).
America, compared genetic patterns This study suggested that the group
with the range of at least one species under study was paraphyletic, which
reaching northern South America.11 As means that more work needs to be done.
we discussed earlier, two species have Numerous other studies suggesting
been recognized because they tend to similar patterns have been published or
occupy separate ranges but show some are underway. One thing these genetic
overlap, where habitat separation occurs. patterns allow us to compare is species
Using sequencing of mitochondrial that occur in allopatric populations, such
genes from samples taken across the as widespread island species. Using
range of the meadowlarks, the research- simple observation, we can always see
ers found that there may really be three differences among island populations
species of meadowlark, with the “new” of such species, but it is impossible to
species occurring in southern Arizona test whether the populations are true
and northern Mexico. Many recent stud- species. With genetic techniques that
ies examining genetic variation within provide quantitative differences in gene
what is considered a single species have patterns to define species, we can com-
shown patterns of genetic variation that pare such island populations and see
justify the naming of new species. how the interisland differences compare
Another study examined the genetic with the differences found between two
relationships among the blue buntings populations that are clearly different
of the genus Passerina and their possi- species. Although we have learned much
ble close relatives.12 We discussed the about species differences using such
Indigo Bunting (P. cyanea) and Lazuli molecular techniques, there is still much
Bunting (P. amoena) earlier when we to learn.
talked about species that had recently The avian tree of life project. As molec-
come into contact as forests spread ular biology advanced, it became easier
across the Great Plains. These spe- to look at longer and longer sequences
cies had hybridized enough that some of base pairs along a segment of DNA.
considered them a single species; some While a few hundred base pairs are
of the other buntings were also known probably sufficient for within-species
to occasionally produce hybrids when or within-genera studies, it also became
together. This study used cytochrome b clear that larger data sets allowed more
and included all six species considered precise and widespread comparisons
to be members of the genus, plus the within the bird world, so that phyloge-
chapter 6

possibly related Blue Grosbeak (formerly nies could be developed that were rele-
Guiraca caerulea), some blue buntings of vant to levels above species and genus.
the genus Cyanocompsa from the tropics, The avian tree of life project

168

1stPages_A.indd 168 7/22/20 11:04 AM

1stPages_A.indd 169 7/22/20 11:04 AM
 involved 18 collaborators who measured Fig. 6.3. A phylogeny for the buntings of the
gene sequences from 169 species of genus Passerina, including the Blue Grosbeak,
birds from all but three nonpasserine formerly of the genus Guiraca. This model
families and all major passerine lin- suggests that the Blue Grosbeak is more
eages, plus two crocodilian outgroups. closely related to the Lazuli Bunting than that
This sequencing targeted the same species is related to the Indigo Bunting. These
locations in the genome and resulted data resulted in putting the Blue Grosbeak
in about 25 kilobases of sequence data into Passerina, although some recent work
suggests that the Indigo and Lazuli Buntings
from each species, which is about five
are more closely related than shown here.
times what was found in previous stud-
The outgroup used to provide scale is three
ies. This impressive data set (over four species of tropical buntings in Cyanocompsa,
million bases in all) was analyzed by including the Blue Bunting (C. cyanoides).
computer and a tree was made showing
relationships among these 169 species.13
These patterns were then assigned from that of Sibley, but it is also one that
taxonomic categories (fig. 6.4) in a way will likely change in the future.
that showed the relationships found in More detailed studies from the com-
this study and compared them to the ponent pieces of the tree of life study
classical phylogeny of James L. Peters have been published. A detailed exam-
(who edited checklists of birds of the ination of the wood warblers (family
world from 1931 to 1979), the tapestry of Parulidae) is remarkable both for those
Sibley, and a recent morphology-based species whose systematic position did
cladistic phylogeny. not change and for those groups that
This study reconfirms the existence saw massive movement in their posi-
of many avian groups at higher taxo- tion relative to other warblers.14 The
nomic levels. Most families that were sequence data showed that the family
described by old-fashioned methods are Parulidae constituted a distinct group,
still families when described by molecu- once a few species were removed that
lar similarity. It is in some of the rela- just no longer fit into this group. The
tionships among groups that surprising species removed from the warblers
results appear. For example, at the very included the Yellow-breasted Chat
top of the figure, we have passerine birds (Icteria virens; which never did look like
closely allied to parrots, and these are a real warbler) and several species from
most closely allied to falcons. Humming- the Greater Antilles of the West Indies
birds end up in a group with swifts, frog- that looked like warblers but did not
mouths, nightjars, and potoos. Several share warbler ancestry. The main group
groups (doves and pigeons, tropicbirds, of remaining warblers was split into two
hoatzin, grebes, flamingos, and sand- parts, one of which was the Ovenbird
grouse) do not seem to be related to any (Seiurus aurocapilla), a sister species to
other group in this system. This amazing all the other warblers. A group of “old”
data set suggests that various ecological warblers that included the Worm-eating
chapter 6

types (waterbirds, raptors, etc.) have Warbler (Helmitheros vermivorus), Swain-

evolved several times in birds. It is a very son’s Warbler (Lymnothlypis swainsonii),
different story from those of the past or Prothonotary Warbler (Protonotaria

170

1stPages_A.indd 170 7/22/20 11:04 AM

 Fig. 6.4. The tree of life phylogeny of birds, by Livezey and Zusi (2007). Note that most
which used large sequences of base pairs to smaller groups remain groups in all systems
show how major groups of birds are related (for example, parrots are always parrots),
and how these groups compare with classical while the most advanced molecular methods
groups (shown as Peters 1931–1979), with have rearranged these groups in many cases
DNA hybridization work (Sibley and Ahlquist (parrots are closely related to passerines in the
1990), and with a recent phylogeny developed newest system).

1stPages_A.indd 171 7/22/20 11:04 AM

 citrea), and Black-and-white Warbler Genomic approaches to systematics
(Mniotilta varia); two waterthrushes and other evolutionary traits
(formerly in Seiurus with the Ovenbird
but now placed in Parkesia); and the Only in recent years have we been able
“winged” warblers (Golden-winged to measure the complete genome of a
[Vermivora chrysoptera] and Blue-winged species, focusing first on humans and
Warbler [V. cyanoptera]) all remained as then on organisms that are important
distinct groups within single-species or to humans for food or other products.
two-species genera. Not surprisingly, the chicken and turkey
The forest understory warblers for- were the first bird species to have their
merly included in the genus Oporornis whole genome measured, along with the
were combined into Geothlypis with the zebra finch.
Common Yellowthroat (G. trichas). The Late in 2014, the journal Science
genus Dendroica kept 24 of its original published a special issue on avian
species, and the Hooded Warbler (Wil- genomes. This package included an
sonia citrina), American Redstart (Seto- introductory overview of genomic
phaga ruticilla), and two Parula species research,15 and 8 papers dealing with
were added to this group. Because the avian genomes. In addition, 20 papers
rules of taxonomy state that the name dealing with related topics appeared
of a genus is established when the first concurrently in other major journals.16
species in that genus is described, and While the focus of much of this work
the American Redstart was the first of was phylogenetic, much of it also dealt
this group to be described, this whole with the inheritance of such traits as
group was put into the genus Setophaga song learning. While the tree of life
and the genus Dendroica disappeared. study used sequencing data gathered
Rearrangements within the warblers by 19 collaborators, the main paper
also led to the loss of the genera Wilso- describing avian genome evolution
nia and Parula. involved 106 collaborators who gathered
Finally, this study showed that information and did genetic compari-
a group of warblers from South and sons for only 48 species. Just the use of
Central America were “good” warblers, the supercomputers needed to do these
but distinct from those found primarily comparisons took several months.
in North America. Similar analyses of While this project was a tremen-
other groups are appearing regularly, dous step forward in our knowledge
changing our understanding of evolu- about avian phylogenies, the truth is
tionary relationships within both what that we still have some way to go until
seemed to be distinct groups and those we have all the proper data. This study
species that always appeared to be a bad included “only” 48 species, although
fit for a particular group. It makes for these covered most of the accepted
exciting times in the systematic world, orders. These species had variable
but it also means one needs to buy a amounts of data; for a few species, the
chapter 6

new field guide pretty regularly. researchers were able to sequence only
about 48 kilobases on average, which is
about double what was studied in the

172

1stPages_A.indd 172 7/22/20 11:04 AM

 tree of life project. Many species had ers performing this next-generation
much larger samples. study selected particularly meaningful
There is general agreement between locations within the genome to do the
the genomic approach and the tree of comparisons and ran huge sequences
life approach, despite the smaller num- of base pairs for each species. Samples
ber of species involved in the genomic involved 259 genes with an average of
approach. Among the most controver- 1,524 bases at each site, for a total of
sial aspects of the tree of life approach 394,684 sites for each species. The most
was the close linkage between parrots advanced Bayesian statistics grouped
and passerines, and between falcons this massive data set.
and seriemas. The genomic approach The general results from this study
reinforces the validity of this grouping, suggested several major groupings for
as it does the close relationship between existing birds, many of which agreed
ducks and chicken-like birds, flamingos with the results of the genome study.
and grebes, and egrets and pelicans, to First, both studies made it clear that
name just a few. A few groups whose the large walking birds (the ostrich,
position was not clear within the tree emu, etc., of the Paleognathae) were
of life now seem to fit into clear clus- closely related to the highly terrestrial
ters that make sense. For example, tinamous (Tinamiformes). Not surpris-
the pigeon/​dove and mesite group is ingly, perhaps, these walking birds were
now clearly allied with the sandgrouse most closely related to a group called the
and closely related to the flamingo/​ Galloanserae, which includes the game
grebe group, but the tropicbird group is birds and waterfowl. These two groups
elsewhere in the phylogeny (and most are considered sister groups to the mod-
closely allied to the sunbitterns). The ern birds, the Neoaves.
hoatzin has been a difficult species to The Neoaves can be split into five
place for decades, but this approach major clades that constitute sister groups
seems to make it clear that it is closely to the rest of the Neoaves (fig. 6.5).
related to cranes and shorebirds. These include (1) a clade that consists
Next-generation DNA sequencing. About of nightjars, other caprimulgiforms,
a year after the genome results were swifts, and hummingbirds; (2) a clade
published, a study appeared that used uniting cuckoos, bustards, and turacos
“next-generation DNA sequencing.”17 with pigeons and sandgrouse; (3) a clade
This massive sequencing study differed including cranes and their relatives; (4)
from the previous two approaches in a a comprehensive waterbird clade includ-
Systematics and Taxonomy

variety of ways. It covered 198 species ing all diving birds, wading birds, and
from all 40 of the recognized orders shorebirds; and (5) a diverse clade that
of birds, with emphasis on nonoscine shows the enigmatic hoatzin (Opisthoc-
groups. This sample size was similar to omus hoatzin) as a sister group to one
that of the tree of life but was about four including raptors, vultures, songbirds,
times larger than the genome sample. parrots, and most terrestrial nonpasser-
This resulted in a smaller sample size ines from owls to woodpeckers.
in terms of base pairs when compared Our ability to measure genetic
to the genomic study, but the research- traits increases daily, so we can assume

173

1stPages_A.indd 173 7/22/20 11:04 AM

 that during the time this book is being relative to other such groups as we gain
produced, advances will increase the more genetic information. For example,
detail of our understanding of avian for the past century, nearly all bird books
phylogenies such that the book may be have started with a look at loons and
out of date as soon as it is printed. On then grebes, but modern systematics
the other hand, we have also seen how shows that these two groups are not at
the larger groups (orders and families) all related; grouping them makes sense
tend to remain as distinctive groups, only because they have converged in
although we have changed their location morphology to make them more sim-
ilar than most bird groups are to one
another. We should expect the future of
Fig. 6.5. Comparison of the major results
systematics to involve a relatively short
regarding the Neoaves from a next-generation
DNA study (left) and a whole-genome study
period to firm up these higher catego-
(right). Note that most of the groupings ries, and then a longer period as we
are similar, although a few show strong develop firm phylogenies through the
disagreement between the two techniques species and even subspecies level.
(Prum, Berv, Dornburg, et al. 2015; Jarvis,
Mirarab, Aberer, et al. 2014).
chapter 6

174

1stPages_A.indd 174 7/22/20 11:05 AM

 Mixed methodologies and system- complex, as it shows only six genetic
atic advances. As we have just noted, species of finches, but these species
advances in technology, primarily the show a great deal of morphological
ability to sequence DNA in the lab and variation from one island to the next.
then the ability to compare sequences The old model of speciation suggests
with supercomputers, have greatly slow rates of change that result in new
changed how we do avian systemat- species, and once a species arises, it
ics. Although DNA hybridization and moves from island to island but does not
modern genomics both deal with the change much as it does so. In contrast,
whole genome, they are very different the new data suggest that there are few
in the sophistication of their results. In real genetic species of finches; rather,
many cases, different methods may lead populations vary from island to island
to different interpretations of data and depending on when they get there and
different hypotheses for phylogenies. what sort of competitors they must deal
As many systematists have worked at with when they do. In the latter case,
various taxonomic levels and times with ecological interactions are much more
such a variety of molecular techniques, important and much more dynamic on
it seems easy to get a bit confused about each island, as species attempt to suc-
how any given study fits into the overall cessfully colonize by interacting with the
scheme of avian systematics. species that already exist on an island
There are many interesting exam- when a new population arrives.
ples of dissimilar results being produced Obviously, these studies were done
by different methodologies, making it well and used what at the time were
hard to be sure which study is the most standard, accepted techniques. As
correct. Earlier, we showed how the molecular techniques become more and
buntings of the genus Passerina were more sophisticated, unusual situations
related, with the Blue Grosbeak of the such as this may appear that will force
genus Guiraca lumped with the other us to change how we think about some
small buntings and moved to Passerina. phylogenies.
A more recent study suggests that the
Blue Grosbeak is not as closely related to Do We Need a Phylogenetic
P. amoena as suggested, although it may Species Concept?
still remain in Passerina.
A more complex example involves As molecular biology became the way
data on the Darwin’s finches of the that most systematists studied bird
Systematics and Taxonomy

Galapagos, a group we discussed ear- phylogeny, broader patterns appeared

lier. A study using fragment length of regarding what sorts of genetic differ-
DNA indicated phylogenetic patterns ences seemed to be correlated with tax-
that match those suggested by clas- onomic differences. Because all genetic
sical morphological studies, with 13 methods produced fairly similar results,
species derived from a single ancestor general patterns emerged as to what
(fig. 6.6).18 In contrast, a more mod- constituted a species as measured by
ern sequencing study of these finches genetic variation alone. Rather quickly,
suggests that the situation is much more a variety of biologists suggested that we

175

1stPages_A.indd 175 7/22/20 11:05 AM

 Fig. 6.6. Comparison of two molecular needed to shift from the biological spe-
techniques used on Darwin’s finches in the cies concept (BSC, as discussed earlier)
Galapagos and the very different results to one that was relevant to the sort of
obtained. The phylogeny on the left side used data being gathered. Most of these ideas
microsatellite DNA length variation, and its fit into what was termed a phylogenetic
results support classical patterns of phylogeny species concept (PSC), where a species
within these species (Zink 2002; Petren, Grant,
is the smallest diagnosable genetic
and Grant 1999). The phylogeny on the right
cluster.19 The PSC has a variety of advan-
used mitochondrial DNA sequences. The
latter suggests a totally different evaluation
tages, chief among them the consistency
of finch phylogeny, indicating that there are that would occur if all taxonomic deci-
fewer genetic lines within this group but much sions were based on similar levels of dif-
more flexibility in morphology as populations ference among groups. In contrast, the
move from island to island (as shown by BSC is often inconsistent, with seem-
colored lines). Names were given only to the ingly arbitrary decisions about whether
conventional classification scheme. two separate populations are the same
species. With the PSC, such situations
chapter 6

never occur, as any two species can be

quantitatively compared.
To date, the BSC has not been

176

1stPages_A.indd 176 7/22/20 11:05 AM

 replaced by the PSC in most cases. 10,473 species of birds in the world from
When finalizing the latest of the Check- 234 families.
lists of North American Birds, the Amer- Avian taxonomy is changing on
ican Ornithological Society committee in an almost daily basis. Two major
charge of those decisions still stated its approaches seem to dominate system-
support for the BSC. Although it is clear atic studies of birds, with one group
that as long as molecular techniques examining the relationships among
dominate systematic methodology, large taxonomic categories (orders and
many systematists will be functionally families) and another group special-
using a PSC, it also seems clear that the izing on categories at the species or
patterns of variation shown by molecu- even subspecies level. The result is that
lar techniques are related to patterns of current taxonomies at the family or sub-
reproduction and distribution across the family level are not clearly defined. We
environment, and these are determined have already discussed how systematic
by the factors that affect the BSC. With studies of the wood warblers resulted in
time, as we develop our understanding some species being removed from that
of both genetic and biological patterns, family, while others were combined into
we should be able to eventually get new genera or species. Checking taxon-
back to agreeing that the BSC not only omy on the websites of the American
works but is supported by the patterns Birding Association and Cornell Lab is
of genetic variation seen in what will probably the best way to keep current
undoubtedly be unbelievably complex with all taxonomic levels. The number
genetic studies in the not too distant of families within each order is shown
future. following the order, and the number
of species within each family is shown
A Taxonomic Classification following the family.
of Birds of the World

The following classification of birds

of the world is based at the order and
family level on The Clements Checklist of
Birds of the World (2007), and the num-
bers of species per family are also taken
from that source. This is the official
world checklist chosen by the American
Systematics and Taxonomy

Birding Association and has been man-

aged by the Cornell Lab of Ornithology.
Both suggest that this is the best possi-
ble source available and that it should
remain so in the future. Taxonomic
categories other than family and order
have been added by the author based on
a variety of other taxonomic works. This
list suggests that there are currently

177

1stPages_A.indd 177 7/22/20 11:05 AM

 class aves: birds
Subclass Neornithes: True Birds
Superorder Paleognathae: Ratites and Tinamous
Order Struthioniformes: Ostriches and Allies (1)
Family Struthionidae: Ostriches (2)
Order Rheiformes: Rheas (1)
Family Rheidae: Rheas (2)
Order Tinamiformes (1)
Family Tinamidae: Tinamous (47)
Order Casuariiformes: Cassowaries (1)
Family Casuariidae: Cassowaries and Emu (4)
Family Dromaiidae: Emu (1)
Order Apterygiformes: Kiwis (1)
Family Apterygidae: Kiwis (5)

Superorder Neognathae: Typical Birds

Order Anseriformes: Screamers, Swans, Geese, and Ducks (3)
Suborder Anhimae: Screamers
Family Anhimidae: Screamers (3)
Family Anseranatidae: Magpie Goose (1)
Suborder Anseres: Swans, Geese, and Ducks
Family Anatidae: Swans, Geese, and Ducks (168)
Subfamily Anserinae: Swans and Geese
Tribe Dendrocygnini: Whistling-ducks
Tribe Cygnini: Swans
Tribe Anserini: Geese
Subfamily Anatinae: Ducks
Tribe Tadornini: Shelducks
Tribe Cairinini: Muscovy Ducks and Allies
Tribe Anatini: Dabbling Ducks
Tribe Aythyini: Pochards and Allies
Tribe Mergini: Eiders, Scoters, and Allies
Tribe Oxyurini: Stiff-tailed Ducks
Tribe Merganettini: Torrent Ducks
Order Galliformes: Chicken-like Birds (5)
Superfamily Cracoidea: Megapodes, Curassows, and Guans
Family Megapodiidae: Mound Builders (22)
Family Cracidae: Guans, Chachalacas, and Curassows (54)
Superfamily Phasianoidea: Grouse, Turkeys, and Quail
Family Phasianidae: Partridges and Pheasants (177)
Tribe Perdicini: Partridges
chapter 6

Tribe Phasianini: Pheasants

Family Odontophoridae: New World Quail (33)
Family Numididae: Guineafowl (6)

178

1stPages_A.indd 178 7/22/20 11:05 AM

 Order Phoenicopteriformes: Flamingos (1)
Family Phoenicopteridae: Flamingos (6)
Order Podicipediformes: Grebes (1)
Family Podicipedidae: Grebes (22)
Order Columbiformes: Pigeons and Doves (1)
Family Columbidae: Pigeons and Doves (342)
Order Mesitornithiformes: Mesites (1)
Family Mesitornithidae: Mesites (3)
Order Pterocliformes: Sandgrouse (1)
Family Pteroclidae: Sandgrouse (16)
Order Otidiformes: Bustards (1)
Family Otididae: Bustards (26)
Order Musophagiformes: Turacos (1)
Family Musophagidae: Turacos and Plantain Eaters (23)
Order Cuculiformes: Cuckoos and Allies (1)
Family Cuculidae: Cuckoos and Allies (146)
Subfamily Cuculinae: Old World Cuckoos
Subfamily Coccyzinae: New World Cuckoos
Subfamily Neomorphinae: Ground Cuckoos and Roadrunners
Subfamily Crotophaginae: Anis
Order Caprimulgiformes: Goatsuckers and Allies (8)
Family Aegothelidae: Owlet-nightjars (10)
Family Podargidae: Frogmouths (15)
Family Caprimulgidae: Nighthawks and Allies (98)
Subfamily Chordeilinae: Nighthawks
Subfamily Caprimulginae: Nightjars
Family Nyctibiidae: Potoos (7)
Family Steatornithidae: Oilbird (1)
Family Apodidae: Swifts (112)
Subfamily Cypseloidinae: Cypseloidine Swifts
Subfamily Chaeturinae: Chaeturine Swifts
Subfamily Apodinae: Apodine Swifts
Family Hemiprocnidae: Treeswifts (4)
Family Trochilidae: Hummingbirds (347)
Order Opisthocomiformes (1)
Systematics and Taxonomy

Family Opisthocomidae: Hoatzin (1)

Order Gruiformes: Rails, Gallinules, Coots, Flufftails, Limpkin,
Trumpeters, and Cranes (6)
Family Rallidae: Rails, Gallinules, and Coots (144)
Family Sarothruridae: Flufftails (12)
Family Heliornithidae: Sungrebes and Finfoots (3)
Family Aramidae: Limpkin (1)
Family Psophiidae: Trumpeters (3)
Family Gruidae: Cranes (15)

179

1stPages_A.indd 179 7/22/20 11:05 AM

 Order Charadriiformes: Shorebirds, Gulls, Auks, and Allies (19)
Superfamily Chionidoidea: Sheathbills
Family Chionididae: Sheathbills (2)
Family Pluvianellidae: Magellanic Plover (1)
Suborder Charadrii: Plovers and Allies
Family Burhinidae: Thick-knees (10)
Family Pluvianidae: Egyptian Plover (1)
Family Recurvirostridae: Stilts and Avocets (9)
Family Ibidorhynchidae: Ibisbill (1)
Family Haematopodidae: Oystercatchers (12)
Family Charadriidae: Plovers and Lapwings (67)
Subfamily Vanellinae: Lapwings
Tribe Hoploxypterini: Spur-winged Lapwings
Tribe Vanellini: Typical Lapwings
Subfamily Charadriinae: Plovers
Family Pedionomidae: Plains Wanderer (1)
Family Thinocoridae: Seedsnipes (4)
Family Rostratulidae: Painted Snipes (3)
Suborder Scolopaci: Sandpipers, Jacanas, and Allies
Superfamily Jacanoidea: Jacanas
Family Jacanidae: Jacanas (8)
Superfamily Scolopacoidea: Sandpipers and Allies
Family Scolopacidae: Sandpipers and Allies (97)
Subfamily Scolopacinae: Sandpipers and Allies
Tribe Tringini: Tringine Sandpipers
Tribe Numeniini: Curlews
Tribe Limosini: Godwits
Tribe Arenariini: Turnstones
Tribe Calidridini: Caldridine Sandpipers
Tribe Limnodromini: Dowitchers
Tribe Gallinagoini: Snipes
Tribe Scolopacini: Woodcocks
Subfamily Phalaropodinae: Phalaropes
Family Turnicidae: Button Quail (16)
Family Dromadidae: Crab Plover (1)
Family Glareolidae: Pratincoles and Coursers (17)
Family Stercorariidae: Skuas and Jaegers (7)
Suborder Alcae: Auks and Allies
Family Alcidae: Auks, Murres, and Puffins (25)
Tribe Allini: Dovekies
Tribe Alcini: Murres and Auks
chapter 6

Tribe Cepphini: Guillemots

Tribe Brachyramphini: Murrelets
Tribe Synthliboramphini: Murrelets

180

1stPages_A.indd 180 7/22/20 11:05 AM

 Tribe Aethiini: Auklets
Tribe Fraterculini: Puffins
Family Laridae: Gulls, Terns, and Skimmers (98)
Order Eurypygiformes: Kagu and Sunbittern (2)
Family Rhynochetidae: Kagu (1)
Family Eurypygidae: Sunbittern (1)
Order Phaethontiformes: Tropicbirds (1)
Family Phaethontidae: Tropicbirds (3)
Order Gaviiformes: Loons (1)
Family Gaviidae: Loons (5)
Order Sphenisciformes: Penguins (1)
Family Spheniscidae: Penguins (18)
Order Procellariiformes: Tube-nosed Swimmers (4)
Family Diomedeidae: Albatrosses (15)
Family Procellariidae: Shearwaters and Petrels (92)
Family Hydrobatidae: Northern Storm-Petrels (18)
Family Oceanitidae: Southern Storm-Petrels (9)
Order Ciconiiformes: Herons, Ibises, Storks, and Allies (1)
Family Ciconiidae: Storks (19)
Tribe Leptoptilini: Jabirus and Allies
Tribe Mycteriini: Wood Storks
Order Suliformes: Frigatebirds, Boobies, and Cormorants (4)
Suborder Fregatae: Frigatebirds
Family Fregatidae: Frigatebirds (5)
Suborder Pelecani: Boobies and Cormorants
Family Sulidae: Boobies and Gannets (10)
Family Phalacrocoracidae: Cormorants and Shags (40)
Family Anhingidae: Darters and Anhingas (4)
Order Pelecaniformes: Pelicans, Herons, and Allies (5)
Family Pelecanidae: Pelicans (8)
Family Balaenicipitidae: Shoebill (1)
Family Scopidae: Hammerhead (1)
Family Ardeidae: Bitterns, Egrets, and Herons (64)
Tribe Botaurini: Bitterns
Tribe Tigrisomatini: Tiger-herons
Systematics and Taxonomy

Tribe Ardeini: Typical Herons

Tribe Nycticoracini: Night-herons
Tribe Cochleariini: Boat-billed Heron
Family Threskiornithidae: Ibises and Spoonbills (34)
Subfamily Threskiornithinae: Ibises
Subfamily Plataleinae: Spoonbills
Order Cathartiformes: American Vultures (1)
Suborder Cathartae: American Vultures
Superfamily Cathartoidea: American Vultures

181

1stPages_A.indd 181 7/22/20 11:05 AM

 Family Cathartidae: American Vultures (7)
Order Accipitriformes: Diurnal Birds of Prey (3)
Suborder Accipitres: Hawks, Eagles, and Allies
Superfamily Accipitroidea: Hawks, Eagles, and Allies
Family Accipitridae: Hawks, Eagles, and Allies (247)
Family Pandionidae: Osprey (1)
Superfamily Sagittarioidea: Secretary-bird
Family Sagitariidae: Secretary-bird (1)
Order Strigiformes: Owls (1)
Family Tytonidae: Barn Owls (18)
Family Strigidae: Typical Owls (209)
Order Coliiformes: Colies and Mousebirds (1)
Family Coliidae: Colies and Mousebirds (6)
Order Leptosomiformes: Cuckoo-Rollers (1)
Family Leptosomidae: Cuckoo-Roller (1)
Order Trogoniformes: Trogons (1)
Family Trogonidae: Trogons (44)
Order Bucerotiformes: Hoopoes and Hornbills (4)
Suborder Upupae: Hoopoes and Allies
Family Upupidae: Hoopoes (2)
Family Phoeniculidae: Wood-hoopoes (8)
Family Bucorvidae: Ground-Hornbills (2)
Family Bucerotidae: Hornbills (59)
Order Coraciiformes: Kingfishers and Allies (6)
Suborder Alcedines: Todies, Motmots, and Kingfishers
Superfamily Todoidea: Todies and Motmots
Family Todidae: Todies (5)
Family Momotidae: Motmots (14)
Superfamily Alcedinoidea: Kingfishers
Family Alcedinidae: Kingfishers (117)
Suborder Meropes: Bee-eaters
Family Meropidae: Bee-eaters (28)
Suborder Bucerotes: Hornbills
Family Coraciidae: Rollers (12)
Family Brachypteraciidae: Ground-rollers (5)
Order Galbuliformes: Puffbirds and Jacamars (2)
Family Bucconidae: Puffbirds (36)
Family Galbulidae: Jacamars (18)
Order Piciformes: Woodpeckers, Toucans, and Allies (7)
Family Lybiidae: African Barbets (41)
Family Megalaimidae: Asian Barbets (34)
chapter 6

Family Capitonidae: New World Barbets (14)

Family Semnornithidae: Toucan-Barbets (2)
Family Ramphastidae: Toucans (36)
Family Indicatoridae: Honeyguides (17)
182

1stPages_A.indd 182 7/22/20 11:05 AM

 Family Picidae: Woodpeckers and Allies (231)
Subfamily Lynginae: Wrynecks
Subfamily Picumninae: Piculets
Tribe Picumnini: Typical Piculets
Tribe Nesoctitini: Antillean Piculets
Subfamily Picinae: Woodpeckers
Order Cariamiformes: Seriemas (1)
Family Cariamidae: Seriemas (2)
Order Falconiformes: Falcons and Caracaras (1)
Family Falconidae: Caracaras and Falcons (65)
Tribe Polyborini: Caracaras
Tribe Herpetotherini: Laughing Falcons
Tribe Micrasturini: Forest Falcons
Tribe Falconini: True Falcons
Order Psittaciformes: Parrots and Allies (4)
Family Strigopidae: New Zealand Parrots (4)
Family Cacatuidae: Cockatoos (21)
Family Psittaculidae: Old World Parrots (180)
Family Psittacidae: New World and African Parrots (168)
Order Passeriformes: Perching Birds (142)
Family Acanthisittidae: New Zealand Wrens (4)
Family Calyptomenidae: African and Green Broadbills (6)
Family Eurylaimidae: Asian and Grauer’s Broadbills (9)
Family Sapayaoidae: Sapayoa (1)
Family Philepittidae: Asities and False Sunbirds (4)
Family Pittidae: Old World Pittas (44)
Family Thamnophilidae: Typical Antbirds (236)
Family Melanopareiidae: Crescentchests (4)
Family Conopophagidae: Gnateaters (11)
Family Grallariidae: Antpittas (55)
Family Rhinocryptidae: Tapaculos (60)
Family Formicariidae: Antthrushes (11)
Family Furnariidae: Ovenbirds and Woodcreepers (303)
Family Tyrannidae: Tyrant Flycatchers (423)
Family Tityridae: Tityras and Becards (33)
Systematics and Taxonomy

Family Oxyruncidae: Sharpbill (1)

Family Pipridae: Manakins (56)
Family Cotingidae: Cotingas (65)
Family Atrichornithidae: Scrub-birds (2)
Family Menuridae: Lyrebirds (2)
Family Ptilinorhynchidae: Bowerbirds (26)
Family Climacteridae: Australian Treecreepers (7)
Family Maluridae: Fairywrens (33)
Family Meliphagidae: Honeyeaters (186)

183

1stPages_A.indd 183 7/22/20 11:05 AM

 Family Dasyornithidae: Bristlebirds (3)
Family Pardalotidae: Pardalotes (4)
Family Acanthizidae: Australian Chats (64)
Family Pomatostomidae: Pseudo-babblers (5)
Family Orthonychidae: Logrunners (3)
Family Cnemophilidae: Satinbirds (3)
Family Melanochartidae: Berrypeckers and Longbills (10)
Family Mohouidae: Whiteheads (3)
Family Paramythiidae: Tit Berrypecker and Crested Berrypecker (2)
Family Callaeidae: Wattlebirds (5)
Family Notiomystidae: Stitchbird (1)
Family Psophodidae: Whipbirds and Wedgebills (5)
Family Cinclosomatidae: Quail-thrushes and Jewel-babblers (11)
Family Platysteridae: Wattle-eyes and Batises (30)
Family Vangidae: Vangas (39)
Family Malaconotidae: Bushshrikes and Allies (50)
Family Machaerirhynchidae: Boatbills (2)
Family Artamidae: Wood-swallows (11)
Family Cracticidae: Bellmagpies and Piping Crows (13)
Family Pityriaseidae: Bristlehead (1)
Family Aegithinidae: Ioras (4)
Family Campephagidae: Cuckoo-shrikes (87)
Family Neosittidae: Sittellas (2)
Family Eulacestomatidae: Ploughbills (1)
Family Falcunculidae: Shrike-tit (1)
Family Pachycephalidae: Whistlers and Allies (56)
Family Rhagologidae: Mottled Berryhunter (1)
Family Oreoicidae: Australo-Papuan Bellbirds (3)
Family Platylophidae: Crested Shrikejay (1)
Family Laniidae: Shrikes (33)
Family Vireonidae: Vireos and Allies (63)
Family Oriolidae: Old World Orioles (36)
Family Dicruridae: Drongos (25)
Family Rhipiduridae: Fantails (53)
Family Ifritidae: Ifrita (1)
Family Monarchidae: Monarch Flycatchers (99)
Family Corvidae: Crows, Jays, and Magpies (128)
Family Corcoracidae: Chough and Apostlebird (2)
Family Paradisaeidae: Birds of Paradise (42)
Family Melampittidae: Melampittas (2)
Family Petroicidae: Australasian Robins (47)
chapter 6

Family Picathartidae: Rockfowl (2)

Family Chaetopidae: Rockjumpers (2)
Family Eupetidae: Rail-babbler (1)

184

1stPages_A.indd 184 7/22/20 11:05 AM

 Family Panuridae: Bearded Reedling (1)
Family Nicatoridae: Nicators (3)
Family Alaudidae: Larks (94)
Family Hirundinidae: Swallows (86)
Family Stenostiridae: Fairy Flycatchers (9)
Family Paridae: Chickadees and Titmice (63)
Family Remizidae: Penduline Tits and Verdins (11)
Family Aegethalidae: Long-tailed Tits and Bushtits (11)
Family Sittidae: Nuthatches (27)
Family Tichidromidae: Wallcreeper (1)
Family Certhiidae: Creepers (11)
Family Troglodytidae: Wrens (85)
Family Polioptilidae: Gnatcatchers (15)
Family Cinclidae: Dippers (5)
Family Pycnonotidae: Bulbuls (143)
Family Regulidae: Kinglets (6)
Family Pnoepygidae: Cupwings (5)
Family Macrosphenidae: African Warblers (21)
Family Cettidae: Bush-Warblers and Allies (36)
Family Phylloscopidae: Leaf Warblers (76)
Family Acrocephalidae: Reed-Warblers and Allies (61)
Family Locustellidae: Grassbirds and Allies (61)
Family Donacobiidae: Donacobius (1)
Family Bemieridae: Malagasy Warblers (11)
Family Cisticolidae: Cisticolas and Allies (145)
Family Sylviidae: Sylviid Warblers (33)
Family Paradoxornithidae: Parrotbills, Wrentit, and Allies (36)
Family Zosteropidae: White-eyes and Allies (130)
Family Timaliidae: Various Babblers (52)
Family Peliomeidae: Ground Babblers and Allies (58)
Family Leiothrichidae: Laughingthrushes and Allies (146)
Family Promeropidae: Sugarbirds (5)
Family Modulatricidae: Dapple-throat and Allies (3)
Family Irenidae: Fairy Bluebirds (2)
Family Hyliotidae: Hyliotas (4)
Systematics and Taxonomy

Family Muscicapidae: Old World Flycatchers (317)

Family Turdidae: Thrushes and Allies (171)
Family Mimidae: Mockingbirds, Thrashers, and Allies (34)
Family Sturnidae: Starlings, Mynahs, and Allies (122)
Family Buphagidae: Oxpeckers (2)
Family Chloropseidae: Leafbirds (11)
Family Dicaeidae: Flowerpeckers (47)
Family Nectariniidae: Sunbirds and Spiderhunters (139)
Family Prunellidae: Accentors (13)

185

1stPages_A.indd 185 7/22/20 11:05 AM

 Family Motacillidae: Wagtails and Pipits (67)
Family Urocynchramidae: Przewalski’s Rosefinch (1)
Family Elachuridae: Spotted Elachura (1)
Family Bombycillidae: Waxwings (3)
Family Mohoidae: Hawaiian Honeycreepers (5, extinct)
Family Ptilogonatidae: Silky-Flycatchers (4)
Family Dulidae: Palmchat (1)
Family Hylocitreidae: Hylocitrea (1)
Family Hypocoliidae: Hypocolius (1)
Family Peucedramidae: Olive Warbler (1)
Family Calcariidae: Longspurs and Snow Buntings (6)
Family Rhodinociclidae: Thrush-Tanager (1)
Family Parulidae: New World Warblers (110)
Family Thraupidae: Tanagers (377)
Family Calyptophilidae: Chat-Tanagers (2)
Family Phaenicophilidae: Hispaniolan Tanagers (4)
Family Nesospinidae: Puerto Rican Tanager (1)
Family Spindalidae: Spindalises (4)
Family Zeledoniidae: Wrenthrush (1)
Family Teretistridae: Cuban Warblers (2)
Family Icteriidae: Yellow-breasted Chat (1)
Family Mitrospingidae: Mitrospingid Tanagers (4)
Family Emberizidae: Old World Buntings (44)
Family Passerellidae: New World Sparrows (130)
Family Cardinalidae: Grosbeaks and Allies (49)
Family Icteridae: Troupials and Allies (105)
Family Fringillidae: Finches, Euphonias, and Allies (225)
Family Passeridae: Old World Sparrows (42)
Family Ploceidae: Weavers (116)
Family Estrildidae: Estrildid Finches (140)
Family Viduidae: Whydahs and Indigo Birds (20)
chapter 6

186

1stPages_A.indd 186 7/22/20 11:05 AM

 C HAP T E R 7

Foraging Behavior

P
revious chapters have examined mining how a bird forages is the distri-
the evolutionary factors that bution of its food. This is true during
led to species of birds and gave both breeding and nonbreeding seasons,
each species its particular phys- but breeding adds some other factors
iological and morphological features. to the decisions a foraging bird must
The morphology of each species can be make. The ways in which breeding and
seen as the set of tools it has available to being tied to a nest site might change
make its living; certainly, anatomy and what is the best behavior for a bird will
physiology set boundaries on the flexi- be discussed in chapter 12. In this chap-
bility of a species in its diet and foraging ter we will discuss the factors important
behavior. We cannot imagine a heron to foraging birds on a day-to-day basis,
trying to forage on small insects in a as well as the behavioral effects of birds
forest, or a warbler wading in tidal flats. being both predator and prey.
Within these constraints, each individual Most of these ideas about the ways
attempts to survive and breed as best it birds best gather food while avoiding
can. One of the keys to success in both being eaten themselves have been devel-
these endeavors is food in sufficient oped in the last 30 years. The models
quantity and of sufficient quality to sur- used are nearly always “optimality mod-
vive. While gathering large amounts of els” that try to show how the decisions
food seems of obvious importance while made by individual birds maximize
a bird is breeding, efficient foraging may benefits relative to costs either over short
be equally important at other times of periods, as in choices about where to
year. It has been suggested that a small feed and what to eat on a particular day,
sparrow spending the winter in southern or over longer periods, as in the decision
Arizona needs to find a seed every one to of whether to defend a fruit tree or seed
two seconds for 10 hours a day to balance patch through the winter. With these
its daily energy expenditure, while titmice models, small changes in food distribu-
during temperate winters may need to eat tions or predator pressures may change
an insect every three seconds to survive. the cost-benefit ratio such that variation
Recent work has shown that even tropical may occur within an individual on even
insectivores must forage for over 90% an hourly basis or over small distances.
of the day to survive. Obviously, there is Extending such potential variability over
little room for inefficiency; a bird must all bird species results in an alarming
continually make the proper decisions array of acceptable behaviors. While
about how to find enough food. some of the general choices available to
The most important factor in deter- birds regarding foods and the reasons

187

1stPages_B.indd 187 7/22/20 11:27 AM

 for these choices can be discussed here, disadvantages of both flocking and some
the reader should keep in mind that to form of territorial spacing.
cover all the possible alternatives would Food distribution and predator
require a whole book devoted entirely to avoidance are the chief factors that seem
this topic. to determine whether a bird will stay
Models of foraging behavior and alone and, usually, defend a territory or
other evolved characteristics are often whether it will join a flock. In general,
discussed in the form of evolutionary when foods are widely dispersed and
strategies, such as optimal foraging fairly predictable in occurrence, some
strategies or optimal reproductive strat- sort of spacing of individuals or pairs
egies. We must remember that individ- is adaptive, while if foods are patchily
ual birds do not really have strategies (irregularly) distributed in both location
in most cases. Rather, natural selection and time of occurrence, some sort of
has favored those birds whose behav- group foraging is preferred. In addition,
ioral characteristics make them most birds that are exposed to predators while
successful in a certain set of ecologi- foraging may have strong pressures in
cal conditions. Given that a variety of favor of group foraging, while those
different behaviors can occur within a less exposed to predators because of the
species living in a variable environment, nature of the habitat or the bird do not
it is sometimes easiest to explain this gain these antipredator advantages by
behavioral variation by considering what joining a flock. Separating the effects of
the best strategy would be for a bird in food distribution from predator pressure
certain circumstances. Although this in flock-foraging birds can be difficult;
often does make the understanding of because a flock can obtain advantages
evolution clearer, in most circumstances for both reasons, a chicken-or-egg con-
the individual bird does not strategize or troversy can result. Much can be learned
make conscious decisions. by observing species that shift between
flocking and some form of territorial
General Patterns of Foraging: behavior with changing seasons, food
Flocks or Territories? supply, weather conditions, and so forth.

While it has been said that “birds of a Costs and benefits of territorial behavior
feather flock together,” we know that
this is not always true. Some species While territorial behavior in birds has
do occur in impressively large flocks, been known for a long time, it was
but others are widely and thinly spaced the work of Jerram Brown (1964) that
across the environment. It appears that identified the ecological and evolution-
one of the first “choices” in the behaviors ary pressures at work in molding this
evolved by a foraging bird is whether to behavior. He presented a general model
go it alone (or perhaps with a mate) or to (fig. 7.1) that involved a cost-benefit
join a group (a flock). A whole gradient analysis to explain territorial behavior.
chapter 7

of flocking behaviors exists, but before The benefits of territorial behavior come
looking at the complexity of this situ- from the acquisition of resources that
ation, let’s look at the advantages and other individuals might harvest if the

188

1stPages_B.indd 188 7/22/20 11:27 AM

 territorial behavior did not occur; the This model can be adapted to any
costs of territorial behavior are those ecological requirement; it does not deal
involved in keeping these competitors just with food. During the nonbreed-
away. As long as the cost of defense is ing season, food is one of the chief
less than the resource reward, territorial limiting factors, and the distribution of
behavior is adaptive. food is important in affecting territorial
Brown’s model points out that both behavior. During breeding, though, the
ultimate (long-term) and proximate distribution of nest sites may be more
(short-term) factors affect this balance. important than the distribution of food
The ultimate factors are evolved char- (see chapter 12).
acteristics of the species’ basic biology Most small birds show some form of
such as reproductive traits and food territorial behavior at some time of year.
habits and typical population densities; In most cases the area defended includes
proximate factors include the state of all the necessities of life, such as food,
aggressiveness of the individual bird, water, and nest sites. Such all-purpose,
competition for resources, and defensi- nonoverlapping territories have been
bility of the resources. designated Type A territories, although
a name such as “exclusive territory” or
Fig. 7.1. Model showing the trade-offs “multipurpose territory” is more descrip-
associated with the evolution of territorial tive. This is the most common territory
behavior, with emphasis on the balance type among temperate-breeding birds.
between defensibility and resource availability When resources are fairly predict-
(Brown 1964). able and uniformly distributed (fig.7.2),

Foraging Behavior

189

1stPages_B.indd 189 7/22/20 11:27 AM

 Fig. 7.2. Model showing how resource
distribution affects the evolution of territorial may even defend a core of its normal
behavior or flock foraging. foraging range, but it overlaps in occur-
rence with other individuals of the same
species. This pattern is called a Type
it is easy to see that benefits of defense B territorial system and occurs among
would exceed costs. During the breed- tropical forest species. Because of the
ing season, when mate defense and great diversity of tropical species, each
more food are required, the balance species is found at lower densities than
would be tilted even more in favor of species living in the temperate zone.
territoriality. What happens to this The costs of defending the resulting
cost-benefit relationship when resources large territory either from widely spaced
become either more thinly distributed conspecifics or from the multitude
or very patchy in occurrence? In the first of coexisting species would be much
case, as resources become less abun- greater than the benefits received from
dant, a bird or pair of birds would need such defense. It is not surprising that
a larger and larger area in order to have such a system occurs in highly diverse
enough resources to survive. At some tropical habitats, but even there, not
point, the costs of defending this area all species have Type B territories. It
(and perhaps the losses to undetected is interesting to note that in tropical
intruders) would be greater than the second-growth habitats or on small
benefits from the resources protected. tropical islands where species numbers
Here territorial behavior should break are lower and densities higher, Type A
down, but the evenness of resources territories are more common.
chapter 7

does not favor a shift to flock foraging. If resources become more irregular
What often happens instead is that the (patchy) in distribution, territorial behav-
bird or pair of birds remains spaced and ior breaks down. If you can imagine a

190

1stPages_B.indd 190 7/22/20 11:28 AM

 grid of territories superimposed on an Characteristics of Avian Territories
irregular patchwork of resources, you Size and shape
can see that some territories would have
no resources at all while others would
.
The tremendous variation in bird char-
have many more resources than could acteristics makes it difficult to generalize
be used by a single bird or pair (fig. 7.2). about territory size and shape. Generally,
If such a bird or pair defended these bigger birds have bigger territories, as
superabundant resources successfully, shown in figure 7.3.1 Carnivores gen-
much would be unused. Most likely, erally have larger territories for a given
though, the pressure from other individ- bird size than seed eaters, probably
uals would make such defense impossi- reflecting reduced energy flow up the
ble. Also, if this patch of superabundant trophic ladder. The number of compet-
resources changed location every week itors with which a species exists may
(e.g., as different trees came into fruit), also affect territory size. This has been
this territorial behavior would not sup- shown for Song Sparrows (Melospiza
port an activity, such as breeding, that melodia) on islands off the coast of
takes more than a week. Such temporal Washington State (fig. 7.4),2 and it is
patchiness of the food supply certainly part of the explanation for the increased
leads to a reduction in the value of a frequency of Type B territories in the
territorial system. A similar reduction tropics, as the number of coexisting
in value may also occur when the nature species in tropical forests often results
of the resource makes defense virtu- in low densities for individual species.
ally impossible. Seabirds or high-fly- The above patterns in territory size
ing swifts would have a difficult time should reflect the cost-benefit relation-
defending the area in which they forage. ships for each individual of a species
While they might chase intruders away and may vary locally. A good territory
such that some spacing would occur should contain a certain minimum
and groups would not form, defending amount of food within some area con-
a stable, classic territory with no way straint. Food supply is generally difficult
to mark it would be difficult. On the to measure, but one study of African
other hand, many of these same species sunbirds (which feed on flowers) sug-
defend nesting territories. gested that they simply defended an
Many other scenarios can be imag- area large enough to give them a cer-
ined where the distribution of a resource tain number of flowers on which they
makes its defense either difficult or could feed.3 Another study showed an
unnecessary. In most cases, the break- inverse correlation between Ovenbird
down of territorial behavior favors (Seiurus aurocapilla) territory size and
some form of group foraging, and this the density of insects found in the leaf
is usually the best way to deal with the litter.4 Among polygynous species such
Foraging Behavior

resource distribution. Before looking as Red-winged Blackbirds (Agelaius

at the options available when territorial phoeniceus), great variation in territory
behavior is not adaptive, let’s take a fur- size and quality has been measured and
ther look at the characteristics of territo- is believed to be the cause of the evolu-
rial behavior. tion of polygyny. When territory defense

191

1stPages_B.indd 191 7/22/20 11:28 AM

 Fig. 7.3. Relationship between
territory size and body weight
for birds with different diets.
Note that herbivores have
their own relationship and
require smaller territories than
predators (Schoener 1968).

Fig. 7.4. Relationship between

territory size and number of
competing species for the Song
Sparrow (Melospiza melodia)
on coastal islands of British
Columbia, Canada (Yeaton
and Cody 1974).

1stPages_B.indd 192 7/22/20 11:29 AM

 has been reduced to only the nest site, often a function of topographic features
the defended area is much reduced and that serve as natural barriers in terri-
may consist only of the area around the torial defense. Thus, a ridge or stream
nest that an incubating bird can peck. may serve as a boundary. In many
In the colonially nesting Adelie Penguin cases only the interactions between two
(Pygoscelis adeliae), individuals prevent territorial birds define the boundaries
other individuals from nesting too close and give the territory shape. An excep-
by stealing the pebbles with which a tional case is the polyhedral territories of
neighbor’s nest is built and incorporat- some Arctic sandpipers. Here, specific
ing them into their own nests. boundaries are often determined by
Territory size may also vary from head-to-head displays between neigh-
year to year or even within a year. Oven- boring males. A male may interact with
birds’ defended territories are smallest one neighbor until they have forged
during incubation, but larger during a straight line that neither will cross.
periods when the territorial male is He will later do the same with another
attracting mates or feeding young. In neighbor until the nice straight lines
some species, territory size varies from form a polygon that defines his territory.
year to year to reflect resource variation Such geometry is a function solely of the
(the densities of many Arctic-breed- uniform tundra surface and the visual
ing shorebirds are highly correlated technique of territorial defense.
with insect densities on the tundra) or
fluctuations in population size (where Territorial acquisition and defense
more birds are forced to divide the same
amount of space). In some species, how- There seem to be no set rules as to how
ever, only small changes in territory size a bird can best obtain its own territory.
occur despite great annual variations in Obviously, it is best to find an unoccu-
the resource base or in population size. pied area and move in and begin terri-
In these cases, large numbers of non- torial defense. Once a bird has occupied
breeding individuals (termed floaters) a territory for a sufficient period, it is in
occur in the area either during the good shape; studies have shown that the
resource peak or in the year following it territory holder wins nearly all confron-
(because of high fledging success during tations with intruders, a phenomenon
the resource peak; see below). Other known as site dominance. Problems
species occupy the same territories for occur when several or, in the case of
many years in succession. These are migrants, many males seek to estab-
often predators such as the Tawny Owl lish a territory at about the same time.
(Strix aluco) or Galapagos Hawk (Buteo Being the first to arrive on the breeding
galapagoensis) that hold year-round ter- grounds helps. This explains why males
ritories and are long-lived. These traits arrive at the breeding grounds before
Foraging Behavior

mean that new entrants into neighbor- females in most cases, but since all the
ing territories are basically “told” their males arrive more or less simultane-
territory boundaries by the established ously, it does not solve the problem of
birds. obtaining a territory. The usual solution
The actual shape of territories is involves displays, singing, and in some

193

1stPages_B.indd 193 7/22/20 11:29 AM

 cases fighting among the males to estab- in, these interlopers are at a distinct
lish some sort of ranking that results in disadvantage. While the territory owner
the most dominant males establishing knows which flowers have been visited,
territories. In most cases, this is a very the intruder does not. Therefore, the
ritualized contest that minimizes injury, intruder forages inefficiently and the
and usually the older bird wins by intim- territory remains economically defensi-
idation. Many cases of injuries caused by ble for the territory holder. At the point
these interactions do exist, however. where the territory is large enough that
This age-related asymmetry in the territory owner cannot reap these
success may be explained in several benefits although it spends much time
ways. The simplest explanation accepts defending the area, territorial behavior
that an older, more experienced, and should break down. Recent work with
sometimes larger male will be able to hummingbirds suggests that territorial
intimidate a younger rival because of his birds may increase the cost of intrusion
age, experience, and size. More complex by focusing feeding efforts early in the
explanations try to compare the costs morning on peripheral flowers. This
and benefits of fighting to young and reduces the value of these flowers for
old birds. Young males are very likely to the rest of the day and helps discourage
have other chances to win a territory so potential interlopers from entering a
that they have more to lose by putting bird’s territory.
too much energy or incurring too much A classic, although exceptional, case
risk in a fight. Older males are in the of territorial acquisition is found in the
opposite situation and thus tend to get cooperatively breeding Florida Scrub Jay
the better territories. The younger males (Aphelocoma coerulescens). As we will see
occupy territories in suboptimal habi- in more detail in chapter 12, this species
tat, spend time as nonbreeding floaters breeds in groups, with one breeding
either remaining outside the breeding pair and several “helpers” that may or
territories or sneaking around within the may not be related to the breeding pair.6
territories, or, in the case of group breed- These helpers apparently occur because
ers, they may serve as helpers within the of a lack of breeding space. Helpers have
older birds’ territories (see chapter 12). a dominance rank, and among their
In some species, this age-related acqui- duties they aid in territorial defense and
sition of territories has led to situations acquisition. Researchers have recorded
where first-year males winter farther instances in which the dominant male
south than older males (see chapter 9) helper has taken over the neighboring
and, in some cases, spend the whole territory when it became vacant. They
first breeding season on what are nor- have also observed instances where the
mally the wintering grounds. helpers increased the group’s territory
A special case of territorial defense size so much that the dominant male
involves what is known as the cost of helper took over part of it as his own ter-
intrusion.5 For hummingbirds or sun- ritory, forming a territory by “budding.”
chapter 7

birds, which defend flowers, it has been Once a male has obtained a territory,
shown that even if the territory is so the boundaries are defined by interac-
large that other individuals may sneak tions with neighboring males. Once

194

1stPages_B.indd 194 7/22/20 11:29 AM

 these are determined, they are gener- “for the good of the species.” The prob-
ally not fought over again. Rather, the lem with this interpretation is that there
territorial males advertise their presence is no mechanism for group selection; if
(and try to attract mates) with “keep “cheaters” defended smaller territories
out” songs or calls. These presumably and produced more young than “popula-
tend to repel any intruding males. We tion regulators,” cheaters would eventu-
will examine the characteristics of these ally predominate in the population. We
songs in chapter 11. need to look at how territorial behavior
is adaptive to the individual, and it is
Territorial behavior and clear that in many cases it is highly
population regulation adaptive. An individual that defends a
territory to breed or to have enough food
We have seen that territorial behavior to survive lives longer and produces
tends to space birds in fairly regular pat- more offspring than one that does not,
terns and in some cases forces individ- so territorial behavior is adaptive.
uals into poorer-quality habitats where This is not to say that territorial
they may or may not breed. Because this behavior does not result in some reg-
territorial behavior may cause very stable ulation of population. In many cases
populations on at least a local level, it it does, particularly on a local scale. In
has been suggested that one of the pur- hawks and owls, for instance, which
poses of territorial behavior is popula- hold year-round territories and are long-
tion regulation (keeping populations at lived, local breeding populations are
levels that do not deplete the available effectively static, barring some severe
resources). environmental change. In the forest
In trying to understand the inter- bird communities studied by Richard
action between territorial behavior and Holmes and his colleagues in New
total population size, we have to be England, breeding bird populations
very careful both in separating cause (measured as the number of territo-
from effect and in applying concepts ries) changed little from year to year,
of natural selection at the individual even when an insect outbreak greatly
level. Early scientists who argued that increased the food supply.7 But when
territorial behavior seemed to regulate floaters and other nonbreeding birds
populations often justified this as being were included in bird counts, total bird
“for the good of the species.” They felt populations did fluctuate and were
that species that spaced themselves out particularly high the year following the
in this way would never overpopulate insect peak, presumably reflecting the
the environment and thus never risk improved nesting success that year.
extinction, while species that did not This suggests that in this case territo-
regulate undoubtedly overpopulated a rial behavior regulates the number of
Foraging Behavior

habitat, reduced resources to disastrous breeding birds, but not the overall pop-
levels, and went extinct. While this may ulation. Since numerous studies have
appear superficially logical, the mech- shown large numbers of nonbreeding
anism suggested is effectively group individuals drifting about, perhaps the
selection—birds defending territories initial conclusion that territorial behav-

195

1stPages_B.indd 195 7/22/20 11:29 AM

 ior regulates populations reflected the regulation, Jared Verner suggested an
difficulties in measuring the density of interesting twist with the idea of the
nonbreeding bird populations. “superterritory.”8 He argued that since
Given that we have set up a cost-ben- selective advantage is based on the rela-
efit model of territorial behavior, a tive frequency of an individual’s genes in
skeptic might ask: Why did the war- subsequent generations, those indi-
blers studied by Holmes not constrict viduals that defend much more space
their territories when the food supply than they need and thus reduce the
was so large that the cost-benefit ratio total breeding population are effectively
had to favor smaller defended areas? increasing their proportion of the gene
Here we must remember that for many pool produced in that year. This “spite-
species territorial behavior must have ful” behavior has been attacked on sev-
a genetic component. Those individu- eral fronts. Studies measuring the cost-​
als that defend a certain-sized territory benefit ratios of territories have rarely
have been selected over the years over shown much excess defended area, and
individuals that defend larger or smaller those cases where it has been observed
territories. We would expect this when may reflect resource variability as noted
resources are fairly uniform from year to above. On more theoretical grounds, it
year. In the case described above, insect has been shown that there are limits to
outbreaks are fairly rare in a habitat that how many large territories will fit into
varies little on an annual basis. In fact, an area. Smaller territories might fill in
ecologists think that the insects space the gaps between these large territories
their outbreaks for long enough periods and reduce the superterritorial birds to
that the birds cannot adapt to them and a small proportion of the population.
eat too many insects. One year with While the more conventional arguments
abundant resources is not long enough for territorial behavior undoubtedly
to change the genetic composition of explain most avian systems, it is not
this community, particularly when the hard to envision at least some situations
resource base returns to normal the where a bird may defend more area than
following year and the only effect of the it actually needs, for the reasons sug-
increased production is a larger num- gested by Verner’s model.
ber of floating birds. As long as such Interspecific territoriality. Because
resource outbreaks are rare, selection ­coexisting species of birds are usually
will favor those birds that show optimal ecologically isolated from one another,
territorial behavior in an average year. they tend to defend territories only
Since some species (such as Great Tits against other individuals of their ­species
[Parus major]) show variation in territory (conspecifics). Adding the need to
size and in density, we might suspect defend a territory against more than
that their resources are more variable, one species would greatly change the
but such comparisons have not been cost-benefit ratio of territorial defense in
made. most situations. There are some cases,
chapter 7

Aware of this problem of short-term though, where two different species

waste of resources and of the previ- may have similar enough habitats and
ous arguments regarding population ­behaviors that they defend territorial

196

1stPages_B.indd 196 7/22/20 11:29 AM

 Fig. 7.5. Classic case of interspecific territoriality some convergence in the signals used.10
between the Red-winged Blackbird (Agelaius The Red-eyed Vireo (Vireo olivaceus)
phoeniceus) and the Yellow-headed Blackbird breeds across most of eastern North
(Xanthocephalus xanthocephalus). Red- America, while the Philadelphia Vireo
wings arrive first and subdivide the marsh into (Vireo philadelphicus) overlaps with the
13 territories, but when yellow-heads arrive, red-eye in a smaller part of the northern
they take over the central portion of the marsh boreal forests. The Philadelphia Vireo
and force the red-wings away from the deeper,
looks like a Warbling Vireo (Vireo gilvus)
more open water (Orians and Willson 1964).
but sings just like a Red-eyed Vireo, and
the birds are interspecifically territorial
boundaries against both conspecifics where they co-occur. Philadelphia Vireos
and heterospecifics. A classic ­example seem to recognize that red-eye songs
of this was recorded in marshes in are different, while red-eyes seem to
­Washington State, where Red-winged treat Philadelphia songs as their own.
Blackbirds (Agelaius phoeniceus) would Both seem to respond to similar habitat
arrive at the marsh first and males would ­preferences.
divide the whole marsh into territories.9 A number of species show interspe-
Later in the spring, the larger and more cific territoriality in the tropics along
aggressive Yellow-headed Blackbirds gradients of changing vegetation. In
(­Xanthocephalus xanthocephalus) would these cases, where species change along
take over the best part of the marsh, the gradient, interspecific territoriality
Foraging Behavior

­forcing the red-wings to shift their occurs at the species’ boundaries.

­territories to the marsh edge (fig. 7.5). We would not expect that a single
If songs or plumage traits are used male of a species could successfully
in territorial encounters between males defend his territory from all other males
of two different species, we might expect of all species. Such attempts would

197

1stPages_B.indd 197 7/22/20 11:29 AM

 involve tremendous costs in terms of flock foraging may make prey easier
energy expenditure, perhaps so much to catch. Examples include foraging
time and energy that the bird would not pelicans and flocks of insectivores that
have enough left to successfully repro- may flush insects toward one another.
duce. Ecologists call the situation where In cases where resource patches are not
a territorial bird spends so much time rapidly renewed, it has been suggested
defending its territory that it reduces that flock foraging increases search
its reproductive success “aggressive efficiency by making it very clear which
neglect.” Although rare, examples of patches have been used such that a
this phenomenon have been observed flock can move rapidly to another site to
among marsh-nesting blackbirds and search for food. There may be adaptive
certain nectarivores. value in flock foraging in relation to
We assume that energetic and learning; young flock members may be
cost-benefit constraints result in birds able to watch older members and learn
defending their territories against only how to forage more efficiently. Flock
one or two species in nearly all cases. foraging may reduce the daily variation
The exception that perhaps proves this in the amount of food an individual has
rule was recently discovered in Austra- available to eat, since the rapid search-
lia, where it was shown that breeding ing of many group members is likely to
groups of Bell Miners (Manorina mela- find food each day while an individual
nophrys) were able to exclude most other searching on its own may not. This
bird species from their territories.11 It makes flock foraging a sort of “bet hedg-
is not surprising that individuals of ing” strategy to avoid hungry days; this
this species are large, breed in groups, aspect of flock foraging is probably more
and occur in rather simple habitats, all important to young or subordinate birds
conditions necessary to shift the costs than to experienced adults. Finally, there
and benefits in favor of defending the is the “information center” effect, where
territory against all intruders. successful group members may lead
other group members to good foraging
Group Foraging sites. This has most often been applied
Advantages of group foraging to colonially nesting birds (see chapter
11) where successful individual foragers
As noted above, group foraging has lead other birds to the scene of their
both resource and antipredator advan- success, but it could also apply where
tages, and these are often difficult to birds share roosting or watering sites—
separate. For resources that are patch- any location where information could
ily distributed in both time and space, be exchanged. The validity of this idea
foraging flocks are better at both find- is currently being debated, but there is
ing them (since a flock can spread out convincing evidence that at least some
and rapidly swing through a habitat species on some occasions exchange
searching for the patches) and using such foraging information, even if they
chapter 7

them (since the increased number of do so unintentionally.

birds can harvest more of the resource Many possible advantages of group
while it is available). In some cases, foraging as a means of avoiding preda-

198

1stPages_B.indd 198 7/22/20 11:29 AM

 tion have been suggested. Several stud- ties that make it hard to locate, thereby
ies have shown that groups are, in fact, protecting the caller, may be the reason
less susceptible to avian predators than many species have adopted similar
single birds (fig. 7.6). The most obvious alarm calls.
reason for this may be the groups’ ability A more active form of deterrence is
to detect predators. With more eyes mobbing and harassing of the predator
searching for danger, it is harder for a by its potential prey. Mobbing behavior
predator to sneak up on its prey. Several represents an attempt to chase the pred-
studies have shown that flock foragers ator away from the area. It apparently
spend less time looking up away from works only because few prey items can
their food than solitary birds, which also be caught by the predator without the
makes the flock foragers more efficient advantage of surprise. When a preda-
(fig. 7.7). In the example shown, total tor initiates an attack, flocks may also
vigilance increases with increasing be advantageous because they either
group size, making each individual both confuse the predator (it does not know
safer and better able to feed. In some which prey individual to attack) or
species, it appears that individuals serve cause it to risk injury. This last advan-
as sentinels, searching for predators tage could apply particularly against
while the others feed. predators such as falcons that make
Once a predator appears, flocks still aerial attacks at high speed and could
have some advantages. In some cases, damage themselves by hitting nontarget
they may passively deter the predator by individuals. Actual examples of these
issuing alarm calls such that all birds in advantages of flocking are difficult to
the area are aware of the predator. This find. Finally, there may be some advan-
may reduce the predator’s effectiveness tages to flock foraging based on laws of
and result in its moving to other areas probability. Being part of a flock reduces
to feed. Since the bird that initially calls the risk to any individual once a preda-
may in fact attract the predator and tor appears, particularly if the individual
increase its likelihood of becoming prey, uses the flock in which to hide. Because
these alarm calls have been of interest flocks are widely spaced, flocking may
to behaviorists. Studies have shown that reduce the frequency of encounters with
the calls are often of a frequency (pitch) predators, although this benefit may
that is hard to localize, thereby reducing be balanced by the increased visibility
the risk to the caller. Call properties have of flocks and the fact that the predator
been noted to be similar among many may more easily follow them than it can
species, so that alarm calls often alert single individuals.
all neighboring birds. Yet whether these Attempts to separate the foraging
calls are made purely for the benefit of component of flocking from the anti-
the individual and its family (which is predator components have met with
Foraging Behavior

often nearby) or for all neighboring indi- many difficulties. Since Hawaii has few
viduals (based on a complex idea known avian predators and birds less com-
as reciprocal altruism) is still under monly flock there, some researchers
study. The fact that the best predator have suggested that predation is the
warning call is one with physical proper- chief selective agent causing flocking.

199

1stPages_B.indd 199 7/22/20 11:29 AM

 Fig. 7.6. Success rates of Merlin (Falco
columbarius) when attacking shorebirds
along the coast of California in winter. Note
that single birds and large flocks are the most
vulnerable groups (Page and Whitacre 1975).

Fig. 7.7. Relationship between predator

vigilance and group size in foraging Ostriches
(Struthio camelus). Each bird in a group
needs to spend less time with its head up
searching for predators, which allows it to
spend more time foraging. Note also that total
vigilance increases with group size (Bertram
1980).

1stPages_B.indd 200 7/22/20 11:30 AM

 Others believe, however, that antipreda- antipredator device and then divide into
tion benefits are simply “gravy” that smaller groups to forage during the day.
accompanies the other advantages of We must remember that the “decision”
group foraging, arguing that flocks form to join a particular flock is made by
primarily for foraging reasons. As with an individual bird, depending on the
so many other ecological patterns, all advantages and disadvantages offered to
these factors are undoubtedly at work in it. This decision will vary depending on
some situations. In trying to understand the bird’s social position in the flock (see
why a particular species forages alone below) and how that affects its ability
or in flocks, we must get some feeling to gather food and avoid predators.
for the predation pressures the species Because such factors as flock size and
experiences, but obtaining accurate field composition, food supply, and predation
measurements of the species’ predation pressures change, the decision that is
risks and resource distribution factors best for an individual bird may change
is a difficult task. Some of the examples as well.
discussed below will show the wide In addition to the factors that influ-
variety of possible solutions that birds ence an individual’s decision about join-
have found to the problem of optimal ing a flock of a particular size, we must
foraging and predator avoidance. also remember the choice of whether or
not to join a flock at all. With so much
Factors affecting flock size variability, it is not surprising that stud-
ies have shown that some species have
Now that we have seen the factors tremendous variation in territorial and
that may favor flock foraging, the next flocking tendencies. The Yellow-eyed
question concerns flock size. What Junco (Junco phaeonotus), for instance,
determines flock size? Obviously, this may change its behavior on a daily basis,
will depend on the factors that favor apparently as temperature variation
flock formation in the first place, with changes the cost-benefit ratio of territo-
food supply the most obvious limiting rial defense.12
factor. When there is not enough food It has been suggested that some
in each resource patch to feed the whole temperate species form flocks in the
flock, flock size should be reduced. In autumn that remain in the winter only
terms of predator defense, the ability to as long as the rich resource patches
detect predators levels off at relatively produced during the summer are pres-
small flock sizes, while the other fac- ent. Once these have been harvested,
tors favoring group formation continue the environment is more uniform in
to increase (slowly) with increasing resource dispersion and individuals shift
group size. At some point on the scale back to territorial behavior. Wintering
of increasing flock size, food supply shorebirds on the California coast may
Foraging Behavior

must become limiting and outweigh be territorial in one habitat during one
the antipredator benefits of joining a stage of the tide, yet forage in flocks
flock. Perhaps this variation in pres- in other habitats exposed by low tides.
sures explains why some species roost Wintering shorebirds in Argentina may
in enormous numbers as an apparent defend small territories to feed, yet join

201

1stPages_B.indd 201 7/22/20 11:30 AM

 flocks at night or when a predator has be enough to explain most dominance
been sighted in an area. Some tropical interactions. Other explanations revolve
birds that are basically solitary and terri- around the idea that older birds are
torial may join flocks that pass through more willing to put out effort (a cost)
their territories. It is not known whether for the benefit (the territory) because
the territorial bird gains either foraging older birds have a lower likelihood of
or predator-protection advantages from future opportunities. Younger birds will
this behavior; it has been suggested probably have future chances, so they
that it is simply finding out where the have more to lose in a fight. In species
flock has gone so that it will not waste where males can attract multiple mates
time foraging there until resources have (see chapter 12), the cost and benefit
been replenished. As avian ecologists differentials of these conflicts may
continue to study foraging behavior, come under intense natural selection
a multitude of twists on flocking and (although these signals may also serve
territorial behavior will probably appear to attract females). In some cases, the
simply because of the complexity of the limit to status signaling occurs when the
factors shaping this behavior. signals attract predators to the signaler
at a rate that does not justify the rewards
Dominance and Status Signaling of the dominance position.
in Flocks and Territories While general correlations between
status signals and age are commonly
The idea of dominance and its role in observed, the only real “rule” involved
territory acquisition has already been in dominance disputes seems to be one
briefly discussed. In the case presented, called site dominance, which states that
the dominant individual acquires the the bird holding a territory is usually
territory more or less by definition, dominant over intruders. Experimenters
although dominance is generally cor- have removed older males from some
related with age and may also be com- territories, allowed younger males to
municated by plumage characteristics, replace them, and then released the
size, song repertoire, or other traits older males. If the time from removal
considered to be status signals. It is was short, the older males expelled the
believed that these signals have evolved young intruders, but if it was over a day,
to provide information about individuals the young birds maintained the territo-
that might be in conflict over a territory ries. Thus, site dominance can overcome
or feeding position. This allows each the general patterns of age-related dom-
individual to evaluate its opponent, inance, but under normal conditions
weigh that information against its own older birds have the advantage.
position, and decide what to do. The It was mentioned in chapter 2 that
ultimate value of this system should many factors determine the coloration
be a reduction in the number of fights and patterns of avian plumages. Status
that occur, as such fights risk long-term signaling is an important factor, particu-
chapter 7

losses for the individuals involved. As larly in determining differences between

we suggested before, the general correla- males and females. Territorial birds that
tion between age and dominance may stay in pairs or small groups throughout

202

1stPages_B.indd 202 7/22/20 11:30 AM

 the year are often monochromatic, with status signals. These males are usually
both sexes having similar coloration physiologically mature and capable of
and plumage patterns. Females that breeding after one year of age, but they
look like males may aid in territorial tend to remain in a female-like plumage
defense, because even though males for two or three years. The usual expla-
are normally dominant over females, nation for this is that they have little
a female that looks like a male and chance to obtain territories in their first
has the advantage of site dominance years, so it is better for them to maintain
can intimidate an intruding male. In the more cryptic plumages of females
many species that are territorial during and increase their chances of being alive
the breeding season but flock during when they are old enough to compete
the nonbreeding period, the sexes are for territories with other males. Among
dichromatic, with males usually brightly the apparent costs of having an adult
colored and females dull colored. The male plumage are increased exposure
bright colors of the males appear to be to predators (if the plumage is colorful
useful as status signals in both territory or involves peculiar adornments) and
acquisition and female attraction. As we increased harassment from other males.
will see in more detail later, these bright Since females are not the risk to a terri-
colors in males reach their peak in those torial male that another male is, young
species in which a male can mate with males resembling females that intrude
multiple females. This sexual dichroma- into a male’s territory are not harassed
tism may be seasonal; many species that as severely as they would be if they were
are territorial as breeders flock during obviously males. This phenomenon of
the winter. In some, the bright breeding delayed maturation is particularly pro-
plumages of the male are replaced by a nounced in polygynous species in which
more female-like appearance when not a few older males participate in nearly
breeding. This may be due to the preda- all the breeding. In these species, young
tion risks associated with being brightly males may retain female plumage for
colored, or it may reflect changes in the several years before attaining the male
sorts of signals a male needs to give status signals and attempting to mate.
when participating in a flock. Other While the above situations seem to
species that flock during the nonbreed- be logical explanations for the occur-
ing season maintain the sexual dichro- rence of delayed maturation in males,
matism, and in a few, the variability both some recent ideas have added new twists
among and within age and sex classes to this tale. Some researchers have
is very impressive. Possible reasons for suggested that delayed maturation in
this are discussed below. some species may be a sneaky strategy
The phenomenon of delayed mat- for acquiring territories that are limited
uration appears to be related to the in availability.13 They argue that these
Foraging Behavior

occurrence of both age-related domi- young males are female mimics, which
nance and the existence of many excess allows them to enter a male’s territory
birds that float about before acquiring without being chased for a long enough
territories. In this situation, males have period that they can set up a territory
evolved delayed acquisition of male and acquire site dominance. This

203

1stPages_B.indd 203 7/22/20 11:30 AM

 argument is supported by the fact that spent fighting, leaving more time and
individuals of these species have very energy for other activities.
different and more cryptic plumages With more complex dominance
when they first leave the nest, and then interactions, we might expect that a
they converge on the female plumage more graded set of status signals would
by the first breeding season. If they be adaptive, such that several grades of
are simply waiting safely for a chance rank could be expressed. Sievert Rohwer
to breed, they should maintain the (1975) and others have argued that
more cryptic plumage. Other behavior plumage variation is more common in
seems to fit this intriguing hypothesis, flocking species than in solitary species
although much additional work needs to to allow more complex social structure
be done to support it. with minimized conflict. Rohwer has
The potential number and complex- done a particularly interesting set of
ity of interactions among individuals is experiments with Harris’s Sparrow
much greater in flocking species. With a (Zonotrichia querula). This species feeds
larger number of individuals all needing in flocks on its wintering grounds and
to be in the optimal position to forage shows great individual variation in the
or avoid predation, conflict is inevitable. amount of black on the head and face
Here, dominance hierarchies are critical (fig. 7.8). Old males have much black
to the smooth functioning of a flock, for and are highly dominant, while young
without some such system there would birds have no black at all and are the
be continuous turmoil. The classic most subordinate flock members. Using
dominance system is the pecking order either bleach or shoe polish, Rohwer
found in chickens. Similar linear hierar- altered the appearance of individuals to
chies have been found in some flocking
species, while in others more complex Fig. 7.8. Variation in the amount of black on
interactions occur. Whatever the orga- the face of Harris’s Sparrow (Zonotrichia
nization, it appears that the dominance querula), which is related to dominance and
system minimizes the time and effort status signaling (Rohwer 1975).
chapter 7

204

1stPages_B.indd 204 7/22/20 11:30 AM

 see how this affected their dominance in group foragers. It also shows how
status. Basically, the general ideas about complex such interactions can be, for
dominance hierarchies were supported, in this case it is apparently the interme-
and the role of the status signals was diate-sized bird that suffers most from
reinforced. Previously subordinate birds feeding within a large flock.
that were given black faces were treated
as dominants by subordinate individu- Mixed-Species Flocks with
als; eventually, some of these black-faced and without Territories
individuals started behaving more like
dominants. Dominants who lost their Just as territorial defense is usually a
status signals were forced into many species-specific trait, many flocks, partic-
more aggressive interactions and a lower ularly in the temperate zone, are com-
final dominance rank. Rather than the posed of a single species. Yet given the
most aggressiveness occurring between various factors favoring flock foraging,
individuals of similar rank (because of there is no reason why this has to occur,
the uncertainty over which should be and mixed-species flocks are common.
dominant), most aggressive encounters Mixed-species flocks might always
occurred between highly dominant and be adaptive as antipredator devices, as
very subordinate individuals. It appears it has been suggested that increasing
that Harris’s Sparrows sometimes group size always reduces predation
behave as bullies! chances by some increment. The value
High dominance status appears to of mixed-species flocks for resource
be highly adaptive, although we must acquisition will vary depending on the
be careful about confusing cause and food habits of the species within the
effect. Wintering dominants often have flock. If the species in a mixed flock have
more body fat and thus survive better. very similar food habits, such flocks
During one of the worst Kansas winters have little advantage over single-species
in history, dominance behavior and food flocks, and the additional individuals
limitation seemed to favor the survival may lead to a more rapid depletion of
of a highly dimorphic subset (in size) of food in an area. If the flock members
House Sparrows (Passer domesticus).14 have similar but not identical food
This could be because large males requirements, they may gain enough of
are always dominant and the smallest the benefits of flock foraging in terms of
females always submissive, so neither resource detection to counteract losses
group spends much time fighting. Thus, of food to similar competitors. With sev-
they fed and survived the harsh Kansas eral species harvesting similar resources
winter, while intermediate-sized birds in different ways, mixed-species flocks
wasted more of their energy on aggres- may clean an area more efficiently than
sive interactions and had higher mor- single-species flocks, making it easier
Foraging Behavior

tality rates. While this may be an excep- to avoid this area later until resources
tional case (most winters in Kansas do have been renewed. If the species in a
not produce such sexual dimorphism), mixed-species flock harvest completely
it shows rather nicely the potential different foods, resource pressures
effects of dominance status on survival are reduced, but it is hard to imagine

205

1stPages_B.indd 205 7/22/20 11:30 AM

 a group of species with such different are available further complicates the
food habits being able to maintain a flock-versus-territory dichotomy. The
flock because each species would have intersection point in this confusing
different requirements for movement. continuum may have been found in
Not surprisingly, flocks with several mixed-species flocks composed of
species usually have rather similar food territorial pairs of up to 12 species of
habits, such that insectivores and frugiv- birds (one pair per species per flock) that
ores flock separately. If food supplies are share identical territorial boundaries
unlimited for a brief period, these costs (fig. 7.9).16 When these flocks meet other
of mixed-species flocks disappear. such flocks at territory boundaries, the
A variety of types of mixed-species various species pairs face off to display
flocks occur in nature. When super- and reinforce the territory margins.
abundant resources are harvested by These mixed-species flocks with territo-
several species (such as a school of fish ries are most often composed of insectiv-
by seabirds), behaviorists often term orous birds, which we know are usually
the grouping of species an aggregation territorial because of the nature of insect
rather than a flock, because it does not distributions. Flocking may allow them
really have any structure or temporal to receive the antipredator advantages
continuity. Real mixed-species flocks of a group while remaining dispersed
have consistent patterns of composi- from conspecifics. Once such flocks of
tion, although drawing the line between similar-sized species form, territorial
aggregations and flocks can be difficult. defense mechanisms probably lead to
The most distinctive trait of mixed-spe- the convergence of territorial bound-
cies flocks is the occurrence of what are aries for flock members. Some recent
termed nuclear species.15 These species work has suggested that mixed-species
seem critical to flock formation and flocks of frugivores may occur, but their
appear to guide the flock’s movements. territories are so large that it is hard to
Nuclear species often have distinctive tell whether the different flocks have
calls or call-notes, or brightly colored nonoverlapping territories.17
rump patches or tails. Both sets of traits While we can construct rather sim-
help keep the flock together as it moves ple hypotheses to explain why a species
through the forest. Trailing species should be territorial or join a flock, this
are generally called attendant species, last example further exemplifies how
although some authors have divided complex the real world is. Some spe-
these into several categories. Attendants cies always flock and some always have
usually do not form flocks themselves territories, but many do a little of each
but will join flocks and follow nuclear during the course of a day, a season, or a
species. Although some attendant spe- lifetime. While these variations are most
cies are nearly always members of for- often compatible with the cost-​benefit
aging flocks, others are territorial birds explanations we offered earlier, they
that join the flocks only as they move show how quickly the factors that are
chapter 7

through the attendants’ territory. weighed in making these decisions can

The discovery that generally terri- change.
torial birds will join flocks when they

206

1stPages_B.indd 206 7/22/20 11:30 AM

 Fig. 7.9. Territories of 25
different mixed-species
understory flocks in Manu
National Park, Peru (Munn
1985).

Optimal Foraging: Specific offspring than those that behave differ-

Decisions on What to Eat ently. While the variation within these
foraging behaviors can be explained
The choice of flocking or territorial by examining strategies, it must be
behavior is just the first of many deci- remembered that this variation is really
sions a bird must make in order to the work of natural selection. Since a
gather enough food. Subsequent deci- complex of factors is involved in dis-
sions involve the choice of foods a bird covering what the “right” decisions
eats, where it searches for them, and so are, recent work on avian foraging has
forth. The questions asked at this level revolved around what are called opti-
are generally the same for all individuals, mal foraging models (OFMs). Tests of
but the best answers vary according to these models have greatly increased our
the type of bird involved, whether young understanding of foraging behavior,
are being fed, and of course the variety of not always because the models were
resources available. correct, but because they have given
We have already shown that on us a conceptual framework with which
Foraging Behavior

many occasions food appears to be a to test and compare field observations.

limited resource. It is assumed that Because these models are often complex
individuals with a particular set of and the field is advancing rapidly, we
behaviors for a certain set of ecological will look at just the general features of
circumstances have more surviving the models and their predictions.

207

1stPages_B.indd 207 7/22/20 11:31 AM

 General optimal foraging models gather the above measurements and
plug them into the equations of the
OFMs attempt to incorporate all the proper OFM to get an answer about the
factors that affect the feeding behavior optimal foraging behavior for the bird
of a particular species. Ideally, this “best” involved. In reality, it does not work like
way should be measured as fitness this because many of these measures are
through survival, reproductive success, often unavailable, either to the observer
or both. Since this is frequently not or to the bird, and just one or two
possible, particularly over short periods, small deficiencies in a model can cause
most studies of OFMs have assumed immense problems. Two basic alterna-
that the best measure to use (what is tive approaches have been developed.
termed the currency) is net energy gain Field biologists have searched for excep-
per unit of time, most often calories tionally simple situations where a single
or kilocalories per hour. These models foraging species may feed on only one
must incorporate a variety of character- or a small number of food items. This
istics of both the food gatherer (usually allows rather detailed measures of each
termed the predator) and its food (often potential food item as well as precise
termed the prey). We must know the measurements of the birds involved. For
energetic costs of each of the numer- example, nectarivores have been used
ous behaviors associated with foraging for studies of territorial behavior because
(flying vs. perching, for example), as they have small territories where the
well as the energetic requirements of the number of flowers being defended can
individual bird. For each food item, we be counted. Because territorial behavior
would like to know its availability (i.e., is just the first level of optimal forag-
how long the predator must search to ing, continuing such studies in more
find a prey item), its accessibility (once detail gives us a better understanding of
found, whether it can be captured by the other aspects of foraging. To do this, we
predator), its ease of ingestion (whether measure aspects of nectar production
the predator can simply swallow the by the flowers involved and look closely
food, or must handle and prepare it at the activity patterns of the territorial
in some special way), and finally, its birds. In another case, a researcher was
net nutritive value (how much of it the highly successful in examining starling
predator can digest). Ideally, in addi- foraging behavior both because the birds
tion to absolute measures for each prey fed in open grasslands and because they
item, we should have relative measures brought the food items back to nest
of the above, since the food gatherer boxes where they could be recorded on
may make its decision about one prey cameras.18 These birds fed on only a few
type based on relative densities of other food types, such that the density of all
types. While much of optimal foraging major foods could be estimated and their
is phrased in terms of predator and prey, distributions studied. Situations like this
we must keep in mind that it covers all are ideal for field observations of optimal
chapter 7

types of foragers, such as seed eaters, foraging and in some cases even permit
nectarivores, and so forth. experimental manipulation, the second
Theoretically, all we need to do is alternative for studying optimal foraging.

208

1stPages_B.indd 208 7/22/20 11:31 AM

 Most experimental approaches to usually do not require extensive pursuit
OFMs attempt to obtain answers to once found. Pursuers generally feed on
small questions that are part of the whole fewer prey types, usually with special-
picture. By eventually understanding ized behaviors necessary for the capture
all the little interactions, scientists hope of these food items. Guilds of insecti-
to understand the larger patterns. They vores show this separation clearly. For
hope that what is often lost in realism example, a gleaner that has already spent
is compensated for in the accuracy of time searching for prey will probably eat
controlled conditions. These approaches any prey item it discovers if capture and
vary from manipulation of field condi- handling time are low, even if this item
tions (such as providing extra food in an is one that would not be considered opti-
area) to aviary experiments that are totally mal; the cost of searching has already
self-contained. A great many of these been incurred, and if the other costs are
aviary studies involve members of the negligible, the bird will benefit from
chickadee family (Paridae), with the Great eating the prey unless it is very small.
Tit (Parus major) the champion partici- In contrast, a sit-and-wait predator such
pant in optimal foraging studies. as a flycatcher expends little energy in
While these approaches to OFMs searching for prey but much in capture;
have various problems (see below), they it might be expected to be much more
have at least been successful in organiz- selective about expending energy to
ing our thoughts and leading us to ask catch prey that is unprofitable. These
good questions. Among a variety of top- examples emphasize that prey size is
ics in addition to the territory-flocking often the most important; within the
dichotomy we discussed above, most of constraints of handling time, big prey is
the discussion has centered around the usually better than small prey.
choice of foods and the decision of when Within a species, several studies
to leave a successful foraging location to seem to have shown optimal selection
look for food elsewhere. of food types. When Great Tits were
offered a variety of food items on a
Optimal food choice treadmill, they generally selected those
that would provide the optimal reward,
The major assumption in food choice is usually larger items.19 If food items were
that the optimal forager should feed on widely spaced, though, the tits tended
prey that gives it the greatest net energy to eat all sizes, which shows nicely that
reward when the total costs of search, the food that is optimal varies with the
capture, handling, and digestion are available food supply. In a field study on
considered. There seems to be consid- the selection of sizes of a certain marine
erable variation in how well birds select worm in the diet of Redshanks (Tringa
foods this way, depending in part on the totanus) (fig. 7.10), when a large variety
Foraging Behavior

type of bird and in part on the other fac- of worm sizes was available, the Red-
tors discussed above. Two major forag- shanks selected large ones and ignored
ing strategies tend to appear. Searchers small ones, but when large ones were
tend to feed on a variety of generalized rare, small worms constituted a larger
prey types that must be discovered but portion of the diet.20

209

1stPages_B.indd 209 7/22/20 11:31 AM

 Large prey items are not always opti- in the one predator–one prey system
mal, especially when they require more shows how complex these studies can
handling or capture time than smaller be. Adding one or two more potential
items. In this case, intermediate prey prey types to the system increases the
sizes may give the optimal reward, as complexity manyfold, for the predator
they provide a better balance of capture must keep track of the relative profitabil-
and ​handling time for the energy gained.
White Wagtails (Motacilla alba) feeding
on dung flies gain the greatest amount of
energy per unit of time when feeding on
intermediate-sized flies rather than on
larger or smaller flies (fig. 7.11).21
While the above studies support the
idea of OFMs, the variability in behavior

Fig. 7.11. How Pied Wagtails (Motacilla alba)

select smaller dung flies (left) and why this
makes sense in terms of caloric rewards versus
Fig. 7.10. Evidence for optimal diet selection in handling time. Small flies are just small flies,
chapter 7

the Redshank (Tringa totanus). Note how this even if they can be easily handled. Large flies
species selects bigger prey when it is available may provide more energetic reward but require
(Goss-Custard 1977). much more handling time (Davies 1977).

210

1stPages_B.indd 210 7/22/20 11:32 AM

 ity of each item, which requires knowing Optimal foraging location
the relative distribution of each. If the
forager is feeding on a food type that is Given that few foragers can continu-
becoming scarcer, it must decide when ally harvest food in the same location,
to shift to an alternative prey. Models for they face decisions about movement
this are quite complex and few detailed to new foraging sites. Since resources
experiments have been performed, but tend to be patchily distributed to some
one of the general mechanisms used in extent even for territorial birds, forag-
prey selection has been known for some ers must decide when it is optimal to
time. During observations of the effects leave one patch (which may have been
of Great Tits on prey populations, it was a successful foraging location until
discovered that rare food types usually most of the resources were harvested)
did not appear in the tits’ diets. As these and look for another. With a broader
types became more common, there look at patch-harvesting decisions, we
would be a point at which they rapidly can derive optimal movement patterns.
became of great importance in the diet, Finally, foragers such as nesting birds
and this increase would continue until that must carry prey back to some loca-
some level of satiation. OFMs explain tion must make decisions about how far
this by showing that at low prey densi- from that location to search.
ties, alternative prey is more profitable, Let us look first at those birds that
while at high densities either handling carry food back to the nest or some
time puts a limit on how many prey other site. This is termed central place
items can be eaten, or the bird simply foraging (CPF), and in many ways it
does not prefer a single-prey diet. At is a simple extension of optimal food
intermediate densities, the bird could choice. Added parameters are the costs
forage optimally and have the greatest in travel time to and from the nest to the
effect on prey densities. The mechanism foraging location, the energy involved in
to achieve this shift in prey use was the flight, and the extra weight carried.
termed the search image. At the point Models and intuition suggest that the
where prey densities were high enough farther the bird must fly to feed, the
that the prey item was optimal for har- greater the food material (termed load) it
vesting, the bird changed its behavior must bring back for the trip to be profit-
to look specifically for that food item. able. Since many species can carry only
The search image allowed the predator one prey item, they should search for
to more efficiently find the prey and at larger prey when farther from the nest.
least approach optimality. While this Carriers of multiple prey items should
phenomenon has been observed in the accumulate larger loads when farther
field on numerous occasions, detailed away. The starling study mentioned
measures to fit OFMs are hard to gather earlier supports these ideas nicely, as
Foraging Behavior

and laboratory experiments are difficult parents tended to eat the small prey
to design. captured and carry only larger prey back
to the nest. Load size increased with
distance, with a sixfold increase in flight
time resulting in a doubling of load size

211

1stPages_B.indd 211 7/22/20 11:32 AM

 (fig. 7.12).22 Similar patterns have been Fig. 7.12. Central place foraging in the
shown for colonially nesting bee-eaters.23 European Starling (Sturnus vulgaris). Note
Obviously, a variety of trade-offs can how load size (measured as the number of
occur here. Shorter trips for small prey prey items in the bill) increases with flight time
may balance longer trips for larger prey, to the foraging area (Tinbergen 1981).
particularly if there are upper limits
to load size. These limits may not be food intake reaches the average of the
related just to how much prey can be habitat in general. At this level, statis-
carried in the bill; they may be affected tical considerations alone suggest that
by the energy needed to fly when heav- movement is likely to lead the birds to
ily loaded. It has been suggested that an area that is at least marginally better
hummingbirds never totally fill their than the previous location. This decision
crops because the cost of flying with that about when to move is often phrased in
much extra weight is greater than the terms of “give-up times,” and it involves
benefit of the extra food. some knowledge about the general
Although it is easy to see how a habitat, for how can a forager know
central place forager can optimize when whether this patch is average without
it knows of a high-quality food patch having foraged elsewhere? The time
within a reasonable distance, how does and energy involved in movement must
it, or any forager on patchy resources, also be balanced with the reduced input
decide when to leave this site of former that a heavily utilized patch provides.
success and search elsewhere, the nor- Obviously, this is a difficult theorem to
mal situation in nature? To answer this reproduce in the field or laboratory. Avi-
question, OFMs have usually invoked ary experiments with Great Tits showed
what is called the marginal value theo- that they foraged in the best area of a
rem (MVT). (Yes, one could design an patchy array of foods and then moved
OFM for a bird that is a CPF and use to the second-best site when the best
chapter 7

the MVT.) This theorem suggests that area had been depleted. This supports
an individual bird or a flock should the MVT and even suggests that the tits
forage in a patch until its net rate of monitor the environment. The MVT also

212

1stPages_B.indd 212 7/22/20 11:32 AM

 predicts that the environment becomes knowledge of the type, quality, and dis-
more uniform with time, and there is tribution of other foods or food patches.
some evidence in support of that. But in This knowledge can be gained only by
general, this theorem is very difficult to sampling, a behavior that is not optimal
study under natural conditions. in the short term but may constitute nec-
If foragers do follow some version of essary noise in a truly optimal system.
the MVT or related OFMs, other behav- Most models focus on energy accumu-
ior can be predicted. We would expect lation, but it is obvious that nutrients
area-restricted searching, that is, a shift must also be a consideration, at least at
to reduced movement when capture suc- times. Thus, behavior that is nonoptimal
cess is high. We might also expect some energetically may be optimal nutrition-
sort of optimal search path. For birds ally. Many attempts to compare foraging
using nonrenewing resources (such as behavior and resource availability have
seeds in winter), this path might reflect failed because it is difficult to measure
the birds’ movements as the marginal true resource availability from the bird’s
values of patches change with the birds’ perspective. We might sample insect or
harvesting activities. For example, a flock seed density, but we do not really know
might leave a very rich patch early in how many of these the foraging bird can
winter because other very rich patches find or how many of these may not be
exist. When the rich patches have all available because of toxicity or other fac-
been depleted somewhat, the marginal tors. Plants and insects often go to great
value of the previously exploited patches lengths to make themselves or their
becomes high again and the flock should products distasteful or cryptic, and this
return. When the resources renew must affect OFMs. OFMs cannot deal
themselves at some rate, an optimal with trade-offs in predator avoidance,
forager should develop an even better territorial, or other behaviors without
knowledge of the optimal “return time” becoming too complex. Finally, there is
to the resource. Ripening fruits or nectar disagreement about how often a bird
in flowers are resources that might be should show optimal foraging behavior.
renewed daily, so it is not surprising that Just as some birds have evolved territo-
individuals or flocks visit sites with these rial behavior that averages resource levels
resources on a regular basis. For hum- over long periods (see above), foraging
mingbirds, a daily routine that involves behavior may be optimal only over evo-
movement from flower to flower is lutionary or other long periods and not
termed trap-lining. during shorter periods.
When we add these criticisms to
Problems with OFMs the complexity already found in the best
OFMs, we might wonder whether they
There has been much discussion about are worth the effort. This author feels
Foraging Behavior

the value of OFMs because they cannot they are, even if none of them proves
capture all the realities of nature without to be a perfect fit to natural conditions.
becoming too complex to be mathemati- They have provided a general conceptual
cally comprehensible. For example, opti- framework with which to organize our
mal food choice and patch choice involve thoughts and direct our studies. Their

213

1stPages_B.indd 213 7/22/20 11:32 AM

 necessary generality has often led to set of questions to pose and an overall
their breakdown in specific studies, but structure of thought.24 The result was
they are still of value. For example, the a detailed hierarchy of the decisions a
starling study found that one of the most breeding starling may make to produce
profitable prey items in the diet fed to as many young as possible (as depicted
young starlings prevented the nestlings in fig. 7.13 for an Eastern Bluebird [Sialia
from forming the normal fecal sac that sialis]).25 This makes OFMs a success
the parents could easily remove from
the nest. Too many of these prey items
led to fouled nests, wet young, higher Fig. 7.13. A hierarchy of foraging decisions for
energy losses, and higher nestling an Eastern Bluebird (Sialia sialis) living in a
mortality. Thus, the actual diet limited typical backyard. After feeding its babies, the
the number of these items despite their bird on its nest box must decide which prey
species to use next, given what it just brought
apparent high value in the model. We
to the nest, as that determines foraging
cannot design general models that
location. Next, it must go where this prey can
incorporate such parameters, yet with- best be located, using long-term information
out these general models this detailed on the profitability of different areas. Finally,
and elegant work on starlings might the bird must decide on exact landing and
have been incomprehensible. Instead, probing sites to find the type of food it wants
OFMs provided Joost Tinbergen with a next (Drent 1978).
chapter 7

214

1stPages_B.indd 214 7/22/20 11:33 AM

 even though the starlings did exactly the
opposite of the theory’s predictions!

Increased Foraging Success

by Using Tools

Throughout this section on foraging we

have assumed that a bird’s morphology
puts constraints on the flexibility of its
foraging technique. In essence, foraging
ability is limited by the tools available
to the bird, and normally these tools are
the structure of the bill, wing, leg, foot,
body, and so forth. While a finch could
eventually evolve a warbler-like morphol-
ogy, and vice versa, this could be done
only over a long period. When a finch is
in an ecological situation where it can
behave like a warbler, the morphological
characteristics of the finch undoubtedly
make it an inefficient warbler, at best. In
a few cases, birds have overcome these Fig. 7.14. A Woodpecker Finch (Camarhynchus
morphological constraints by using pallidus) using a cactus thorn to probe for
objects other than their bodies as tools. insect larvae while foraging in a rotting tree.
The classic case of tool use among
birds is the Woodpecker Finch (Cama-
rhynchus pallidus) of the Galapagos when Northwestern Crows (Corvus cau-
Islands (fig. 7.14). This species uses rinus) drop mussels on stones to break
long, sharp twigs to poke into crevices the mussels open.
or holes in the ground and capture prey While tool use is rather a special
that it otherwise could not reach. It may case, it may be an important adapta-
be occurring in the place of woodpeck- tion to those species in which it occurs.
ers, which do not occur on the isolated An OFM for these species would have
Galapagos Islands. Several other cases to consider the cost-​benefit ratio of
have been reported where birds use this behavior with different prey types
sticks to capture prey, with examples and add this trade-off to the ones we
ranging from chickadees to the Green discussed above. Foraging behavior is
Jay (Cyanocorax yncas); new species are one of the most active areas of study in
added regularly. contemporary ornithology. While the
Foraging Behavior

Stones are also used as tools by a findings will undoubtedly be complex

few species. Egyptian Vultures (Neo- and vary from species to species, tre-
phron percnopterus) will drop stones on mendous advances have been made in
ostrich eggs to crack them open. Other recent years and this movement should
species use stones more passively, as accelerate with time.

215

1stPages_B.indd 215 7/22/20 11:33 AM

 CH A P T E R 8

Adaptations for Survival

in Extreme Environments

M
ost avian foods are at least of coping with a variable environment.
occasionally hard to find Before we examine these adapta-
in sufficient quantity or tions, the high energy requirements
quality so that even by of birds discussed in chapter 2 must
optimal foraging, a bird has difficulty be recalled. Birds have some of the
maintaining a positive energy balance highest metabolic rates found among
through the period of scarcity. When animals. These rates are a consequence
this occurs, the bird must use other of their endothermy, of the high level of
mechanisms to aid its survival. When body temperature they maintain, and
these food shortages are regular and of their large surface-area-to-volume
long term, as in many seasonal environ- ratios, which accentuate the rate of heat
ments, one option for a bird is leaving lost compared to the heat produced by
the environment—migration, a topic their small bodies. Recall that avian
covered in chapter 9. This chapter metabolic rates increase markedly at
looks at how birds that stay put sur- environmental temperatures below and
vive extreme conditions where food is above their thermoneutral zone (see fig.
difficult to find. These conditions may 2.23), and that weight-relative metabolic
vary from a daylong shower in a tropical rates increase with decreasing body size
rainforest that keeps a bird from forag- (fig. 2.22). In addition, daily metabolic
ing effectively to the extreme cold of a expenditures of birds are compounded
temperate winter day, where a bird faces by flight, which may increase metabolic
subzero temperatures and a short day- rate by 9–12 times the basal rate. All in
light foraging period. Water can also be all, birds exhibit an expensive lifestyle,
limiting to birds; some of the ways that yet that lifestyle serves to make them
birds have adapted to extremely hot and distinctive and successful in most envi-
xeric environments are considered. A ronments.
few species deal with longer-term varia-
tion in food supply by staying in a region Short-Term Adaptations
but storing food; this chapter finishes to Food Shortage
with a look at food-storage strategies and
at adaptations of memory and sociality Optimal foraging was defined as for-
that may be associated with this means aging behavior that maximizes the net

216

1stPages_B.indd 216 7/22/20 11:33 AM

 gain of calories over time spent forag- cies, such as Black-capped Chickadees
ing. Because a bird engages in activities (Poecile atricapillus), White-breasted and
other than foraging, we expect that most Red-breasted Nuthatches (Sitta carolin-
individuals apportion foraging and ensis and S. canadensis), and Oak Titmice
other behavior in such a way that they (Baeolophus inornatus), which are insec-
maintain a zero net energy balance over tivorous during the summer, switch to
a period such as a day. With conditions a predominantly seed diet during the
that make food more difficult to har- winter. This has two potential benefits:
vest or that require more food, the first seeds may be a more clumped resource
adjustment is to shift this time budget than animal matter, which reduces the
to increase foraging time, with less time foraging cost, and seeds tend to have
spent in other behaviors. a higher fat content than most animal
Species that face periods of food matter (except pupae), so there is a
scarcity with any regularity may adopt greater energy gain per gram of food.
several strategies. One solution is to Such adjustments help most species
store fat during good periods that can survive short periods of food limitation.
then be mobilized as an energy source Among the very smallest of birds,
during leaner times. Birds can lay down the surface-area-to-volume ratio prob-
and mobilize fat rather easily, but the lem may be so extreme that even these
costs of flying with the extra weight limit behavioral adjustments do not suffice
the practicality of this solution. The to allow the bird to survive through
small size and high metabolic rates of the night. In these cases, the bird may
birds also limit the value of this strategy be forced to lower its metabolic rate
over longer periods for many species. during the nighttime hours, a condition
For example, a 25 g bird can store only known as torpor. Many hummingbirds,
enough fat for approximately two nor- the smallest birds in the world, adopt a
mal days of activity, whereas a 2000 g strategy of going into torpor each night,
Turkey Vulture (Cathartes aura) can even in relatively warm environments.

Adaptations for Survival in Extreme Environments

survive a 17-day fast.1 The costs of homeothermy in a 3 g bird
Shifting foraging strategies can may exceed the bird’s energy reserves so
save energy. In some cases it may be that a normal metabolic rate cannot be
energetically less costly for a bird to maintained through the night, making
simply not forage during a brief period torpor a necessity. Generally, though,
when food is difficult to find (such as birds larger than 20 g do not make such
during a shower) rather than pay the an adjustment under normal climatic
high energetic costs of searching with conditions.
limited chance for success. If the bird
spends this inactive period roosting in Survival Adaptations
a protected location, this can lower the for Cold Conditions
energetic costs even further. Starved
Great Horned Owls (Bubo virginianus) Most birds that breed in temperate or
reduce their daily activity time compared boreal zones do not spend the winter
to periods when they feed regularly. there; rather, they fly south to where
Many small northern-temperate spe- food is more readily available. Yet a

217

1stPages_B.indd 217 7/22/20 11:33 AM

 number of species do survive the long and the external heat of the environment
winter season, with its cold tempera- are exchanged by the physical processes
tures, heavy snow cover, and limited of radiation, convection, conduction,
daylight hours for foraging. and evaporation. The direction and
Among endothermic animals, con- magnitude of heat transfer, of course,
servation of heat can be maximized by depends on the thermal gradient.4 In
minimizing the surface-area-to-volume winter, the bird radiates heat from its
ratio. Consequently, cold climates tend warmer surface to the cooler objects in
to be populated by the larger members its environment, conducts heat from the
of a species (Bergmann’s rule), and indi- surface of its warm extremities to any
viduals tend to have shorter extremities cooler surfaces it touches, and has some
than those living in warmer climates heat carried away by convection, that is,
(Allen’s rule).2 Using wing length as by wind moving across the warm skin
an intraspecific indicator of body size, or feather surfaces. Little heat is lost
researchers found gradually increas- by evaporation at low temperatures in
ing size clines moving northward and winter. Birds have some control over the
westward from Florida in Hairy and magnitude of loss via each of these ave-
Downy Woodpeckers (Picoides villosus nues of heat transfer: by morphological
and P. pubescens), Blue Jays (Cyanocitta adaptations that affect plumage density,
cristata), Carolina Chickadees (Poecile penetrability, and color; by behavioral
carolinensis), White-breasted Nuthatches strategies that minimize heat loss; and
(Sitta carolinensis), and Eastern Mead- by physiological mechanisms for con-
owlarks (Sturnella magna). Even among serving heat and/​or augmenting heat
migrants, such as the Song Sparrow production.
(Melospiza melodia), larger individu-
als tend to remain farther north than Morphological adaptations
smaller ones.3 However, these are not
absolute laws but generalizations. There Morphological adjustments are among
are many exceptions to the rules among the most energetically conservative of
endotherms, and interestingly, there are the adaptations to cold conditions, as
also many examples of conformance to all individuals of a species in a region
Bergmann’s and Allen’s rules among possess them and they are relatively
“cold-blooded” vertebrates and even in constant through all conditions in
plants, which do not regulate their tem- winter. Since feathers provide most of
perature. a bird’s insulation, birds that winter to
Although many overwintering the north usually have more feathers per
northern residents are larger species, unit of body weight than more southerly
a number of small (< 20 g) birds such distributed individuals. Species such
as chickadees and finches are able to as chickadees, creepers, and kinglets
survive these conditions. How do they are the smallest of temperate wintering
chapter 8

do it? All animals live in a complex birds, and they are distinctive for having
thermal environment with which they the highest ratios of feather weight to
exchange heat. Internal heat, produced body mass (table 8.1), averaging 10%–
by metabolic processes or by shivering, 11%, compared to an average of 6%–8%

218

1stPages_B.indd 218 7/22/20 11:33 AM

 for other avian species. Chickadees in reflectivity of the plumage. Some birds
particular exhibit a prolonged postnup- that winter in the north have dark plum-
tial molt of some of the body feathers so ages that absorb more radiant energy,
that new feathers are still growing out in and heat gained from insolation (solar
the fall. This ensures less feather wear radiation) reduces the amount of heat
before winter and thus greater insula- the bird must produce internally (i.e.,
tion quality of the plumage. its metabolic rate). As a test of whether
The magnitude of heat loss by radi- plumage color had an effect on bird
ation from a bird’s surface is a property metabolism, an experiment compared
of the transparency, absorbency, and metabolic rates of albino Zebra Finches

Table 8.1
Feather weight as a percentage of body weight in selected groups of birds
family mean % plumage overwinters in
in family temperate zone
Trochilidae 6 N

Picidae 8 Y

Alaudidae 9 Y

Paridaea 10 Y

Sittidae 9 Y

Certhiidae 11 Y

Cinclidae 6 Y

Adaptations for Survival in Extreme Environments

Troglodytidae 8 N

Sylviidae 11 Y

Motacillidae 7 N

Bombycillidae 7 Y

Laniidae 8 Y

Parulidae 9 N

Icteridae 7 N

Fringillidaeb 9 Y

Source: Turcek, 1966.

a
Highest value obtained from 249 species was for Parus major (12%).
b
Some cardueline finches = 11%.

219

1stPages_B.indd 219 7/22/20 11:33 AM

 (Poephila guttata) and albino Zebra for roosting sites when the caves are
Finches dyed black when both were warmer than the outside environment.
exposed to artificial sunlight at mod- Common Redpolls (Carduelis flammea)
erately cold (10°C) temperatures.5 The and even birds as large as Ruffed Grouse
researchers found that the black-dyed (Bonasa umbellus) burrow into the snow
albino Zebra Finches exhibited a 23% and use it as insulation from the colder
reduction in metabolic rate compared to temperatures of the open air. Some spe-
their undyed counterparts. However, the cies other than cavity nesters are known
advantages of being dark are reduced to use old nests for protected roosting
under windy conditions (see below). sites. The Sociable Weaver (Philetairus
Skin is far more transparent to heat than socius) constructs rather mammoth
a layer of feathers is. Obviously, one way nests during the breeding season that
to conserve heat in the cold is to reduce serve as insulated roost sites during
the amount of exposed skin. As much as the nonbreeding season.8 Communal
56% of a resting bird’s heat loss occurs roosting (see below) in the nests further
through the legs, and an additional enhances the birds’ ability to keep the
5%–10% occurs from the mandibles.6 roost site well above ambient tempera-
Because the bare extremities are primary ture; bluebirds (Sialia spp.) may pile
sites of heat loss, birds that winter in the into a cavity together, often with females
north often have feathered tarsi or facial on the bottom and males on top (fig.
areas for insulation. 8.1). Any location that shelters the bird
from cold and especially wind will help
Behavioral adaptations conserve energy. Even a small difference
can be important, given the rather steep
A variety of behavioral modifications can increase in metabolic rate with decreas-
also reduce the cost of existence in the ing temperatures and increasing wind
cold. An individual can select a microen- velocity.
vironment for roosting that minimizes A roosting bird can further reduce
the difference between its body tempera- heat loss by minimizing its surface-­area-
ture and that of the external environ- to-volume ratio with postural adjust-
ment. Researchers calculated that House ments. Most birds that roost in cold
Sparrows (Passer domesticus) could save conditions assume an almost spherical
13.4% of the energy costs of nocturnal shape by tucking the head under the
thermoregulation by roosting in a nest wing and perhaps drawing one foot up
box at subfreezing temperatures (−8°C).7 into the breast feathers (fig. 8.2). This
Because of the bird’s movements inside minimizes the surface area for heat loss.
the nest box and the box’s insulation, To further reduce this loss, some species
the sparrows kept the interior of the box use communal roosts. Here, a number
6°C warmer than the air outside. Cav- of individuals of the same species may
ities in trees provide highly protected roost together, either in the open or in
chapter 8

roosting sites, as do coniferous trees or a cavity. Putting several birds together

other vegetative cover. Andean Hill- greatly reduces the surface-area-to-vol-
stars (Oreotrochilus estella, a species of ume ratio (fig. 8.3). Creepers do this in
hummingbird) are known to use caves the open, putting their heads together

220

1stPages_B.indd 220 7/22/20 11:33 AM

 Fig 8.1. A group of Eastern Bluebirds (Sialia toward the center of the mass, as the
sialis) roosting in a nest box in winter to head is an important site of heat loss.
save heat. Note that males tend to be above The tiny (5.5 g) Common Bushtit (Psal-
females. triparus minimus), although not found

Adaptations for Survival in Extreme Environments

in temperate areas with extreme tem-
peratures, does inhabit cool oak-chap-
arral environments and commonly
roosts communally at temperatures
near freezing. A pair of bushtits roost-
ing together at 10°C expended 18% less
energy than a single bushtit did at the
same temperature.9 The savings would
be even greater at lower temperatures.
Pygmy Nuthatches (Sitta pygmaea) often
roost in large flocks within cavities,

Fig. 8.2. An American Oystercatcher

(Haematopus palliatus) burying its face and
bill in its back feathers and standing on one leg
to save energy.

221

1stPages_B.indd 221 7/22/20 11:34 AM

 thereby adopting at least two strategies Greater Roadrunners (Geococcyx cali-
to conserve energy during the cold fornianus) face away from the morning
winter nights that occur in their moun- sun and spread the back feathers to
tain habitats. Even birds as large and expose bare skin with dark pigmenta-
as well insulated as Emperor Penguins tion. This behavior rapidly warms the
(Aptenodytes forsteri) rely on huddling to bird.10 Dark-plumaged Turkey Vultures
reduce their energy expenditure during (Cathartes aura) and anis (Crotophaga
cold exposure. While the metabolism spp.) are also noteworthy for their bask-
of penguins at the center of the huddle ing behavior during the morning.
may be at or below the resting level (it is
lower in hypothermic birds), the pen- Physiological adaptations
guins at the periphery of the huddle are
noticeably shivering, thereby incurring Physiological adjustments to cold
increased metabolic cost. involve mobilization of energy reserves
Some species may use postural to fuel the high intensity of heat pro-
adjustments during the day to either duction necessary to maintain body
minimize energy loss or maximize gain temperature. Some species of small
from sunlight during cool conditions. cardueline finches have impressive
heat production capabilities. Ameri-
Fig. 8.3. A group of European Bee-eaters can Goldfinches (Carduelis tristis), for
(Merops apiaster) roosting side by side to example, can maintain a constant 40°C
save energy by reducing the amount of surface body temperature for eight hours at
exposed relative to the size of the birds. −70°C (fig. 8.4).11 To maintain their body
chapter 8

222

1stPages_B.indd 222 7/22/20 11:34 AM

 Fig. 8.4. Seasonal variation in the capacity of
high-intensity heat production of an American
Goldfinch (Carduelis tristis). As ambient
temperature is reduced (green), metabolic rate
(blue dots) increases. In summer (red dots),
this increased metabolism can be maintained
for only an hour.

temperature in such extreme cold, these

Adaptations for Survival in Extreme Environments

birds shiver intensely and produce heat
at a rate four to five times their basal
rate. The ability to sustain this high rate
of heat production is seasonal, perhaps
triggered by photoperiod, since sum- of these finch populations. They seem
mer-acclimatized goldfinches are unable to be constantly on the move to find
to sustain such a high rate of metabo- enough food and to make enough fat
lism for more than an hour, after which each day to survive the night. These
they rapidly become hypothermic. To birds also have paired crops that allow
expend this much energy at night, the them to store some seeds for digestion
birds must put on fat during the day that later in the night, effectively increasing
amounts to 15% of their body weight. the period during which food enters the
Accumulating this much fat from a digestive tract.
diet of seeds means finding fairly rich Other species respond physiolog-
food sources, which may be one factor ically to cold in a very different way,
responsible for the irruptive behavior allowing their body temperature to

223

1stPages_B.indd 223 7/22/20 11:34 AM

 Fig. 8.5. Comparison of (a) metabolic rate
and (b) body temperature of a Fiery-throated
Hummingbird (Panterpe insignis) at rest
(dashed line) and in torpor (solid line).
Below ambient temperatures of 12°C, torpid
hummingbirds regulate their body temperature
by increasing their metabolic rate. From 12° to
24°C, body temperature is essentially identical
to air temperature.

mia. The energetic benefit of hypother-

mia or torpor over normothermia can
be seen in figure 8.5.12 A hummingbird
fall below normal during the inactive that spends part of the night in torpor at
period of the day. This decreases the 12°C expends about 1/10 as much energy
temperature gradient between the bird’s as a normothermic individual (which
core and the ambient air, therefore regulates its body temperature at 40°C).
resulting in a slower rate of heat loss Black-capped Chickadees overwintering
and a consequent lower cost of ther- in New York State drop their body tem-
moregulation. This solution to food perature as much as 10°C during cold
shortage can involve either a regulated nights. This reduction in body tempera-
hypothermia, where the body tem- ture lowers the metabolic expenditure
perature is lowered 5°–10°C, or torpor, for the night by as much as 23%. For
where the body temperature is allowed such species, this conservation of energy
to fall to a temperature approaching the is necessary because evening fat reserves
chapter 8

ambient temperature. Torpor is found are insufficient to carry the bird through
only in hummingbirds, swifts, and some the night. The bird must also have some
caprimulgids, while many other species energy reserve remaining to fuel its
exhibit moderate nocturnal hypother- early morning foraging.

224

1stPages_B.indd 224 7/22/20 11:35 AM

 Fig. 8.6. Metabolic rate of an
adult Black-chinned Hummingbird
(Archilochus alexandri) weighing 2.8
g, at 26°C room air temperature over
a 24-hour period. Note that the bird
maintains a normal body temperature
(normothermic) for several hours after
dark and then enters torpor. Arousal
occurs before lights come on at 6:00
a.m.

Adaptations for Survival in Extreme Environments

In many of the species exhibiting they maintained a hypothermic body
torpor, the bird appears to monitor both temperature between 34° and 40°C for
the external stresses and its internal most of the night and entered torpor for
reserves to adjust its body temperature only a short period, arousing to nor-
to a level that leaves some fat reserve mothermia before the lights came on
for the morning. One study found that again (fig. 8.6). Arousal from torpor was
hummingbirds (kept in cages in envi- accomplished by intense shivering heat
ronmental chambers) regulated body production that raised the body tempera-
temperatures of 24° to 43°C overnight, ture about 1°C per minute in these small
adjusting their metabolism to suit individuals. Since arousal occurred in
their energetic reserves.13 They did not the absence of any external stimulus, it
enter torpor every night, nor did they presumably was initiated by an endoge-
become torpid immediately after the nous daily rhythm.
lights went off in their cage; occasionally Many mammals have evolved

225

1stPages_B.indd 225 7/22/20 11:35 AM

 adaptations for long-term torpor, called been known to maintain torpor for up
hibernation, but utilization of torpor for to three months. This long-term torpor
more than one day occurs in only one (or hibernation) allows an aerial insecti-
family of birds, the Caprimulgidae. The vore to survive cold periods in the desert
best example is the Common Poorwill when its food resource (flying insects) is
(Phalaenoptilus nuttallii), a caprimulgid unavailable.
found in the western United States Although lowering body tempera-
and Mexico. When this fairly large ture seems to be an excellent solution to
(75 g) insectivore enters torpor, its body energy limitations, there must be associ-
temperature may drop as low as 6°C ated physiological characteristics, hidden
when the air temperature is near 0°C.14 risks, or some other explanation for why
This, of course, allows it to survive it occurs in only a small proportion of
using very little energy (fig. 8.7). Torpid avian species. True torpor has not been
poorwills usually arouse spontaneously found in any passerine species; noctur-
about every four days, but they have nal hypothermia has been reported in

Fig. 8.7. Variation in

metabolic rate (oxygen
uptake, solid line) and
body temperature (dotted
line) of a Common
Poorwill (Phalaenoptilus
nuttallii) at the beginning
and end of a typical torpor
cycle (Withers 1977).
chapter 8

226

1stPages_B.indd 226 7/22/20 11:35 AM

 only a few passerine species. Why don’t in cool water. For example, the heat
all avian species exhibit wide diurnal loss from one leg of the heron (Ardea
variability in body temperature? Cer- cinerea), which also has a rete, was less
tainly, there seems to be a strong correla- than 10% of the heat production of the
tion between diet and the physiological bird while it was standing in 4°–12°C
strategies used. A redpoll or goldfinch water.16 Heat loss from extremities can
with access to large quantities of fat-rich also be reduced if there is a drop in body
seeds can store and mobilize enough temperature or a sudden immersion of
energy to maintain body temperature the foot into freezing water by sharply
through the night, while a chickadee reducing the blood flow to the foot
feeding on a more depauperate resource (vasoconstriction). However, this is only
of insects and seeds may not harvest a temporary solution and must be fol-
enough food during the day to build an lowed by intermittent blood flow (vaso-
adequate energy reserve for regulation dilation) to the foot in order to prevent
of normothermic body temperature. anoxia and freezing of the tissue.
By dropping its body temperature, the Even with all these possible adapta-
chickadee can survive using about half tions, life during a cold winter is difficult
as much energy as the goldfinch. for birds. Mortality rates of 50% are not
Another physiological adjustment unusual for Black-capped Chickadee
used to conserve heat during cold expo- populations wintering in the north,
sure is countercurrent heat exchange although many of these deaths are
in the extremities, especially the legs. attributed to first-year birds that may be
Heat exchange between the major artery excluded from good roosting sites and
and vein in the limb allows the arterial feeders by the older adults. Perhaps even
blood to cool gradually as it passes to more damaging to bird populations are
the foot, at the same time warming the unseasonal bad weather and cold spells.
venous blood as it returns to the heart. Many of the adaptations discussed
In this way heat loss from the bare above are seasonal, apparently achieved

Adaptations for Survival in Extreme Environments

extremity is reduced because the sur- through hormonal control triggered by
face temperatures are lower. In Giant photoperiod. Thus, an early autumn
Petrels (Macronectes giganteus) there is a frost might kill birds that could easily
marked increase in the temperature of survive the same temperatures later in
the venous blood as it travels up along the season.
the naked portion of the metatarsal,
from the web (10°–15°C) to the feath- Adaptations to Heat
ered portion (> 30°C).15 In long-legged
wading birds such as the Wood Stork For a variety of reasons, hot tempera-
(Mycteria americana), a specialized tures can be as difficult for birds to adapt
vascular structure called a rete is pres- to as cold. That is to say, control of heat
ent in the thigh. The rete consists of a loss to a cold environment is easier to
network of intermingling arteries and manage than control of heat gain from
veins that exchange heat, thereby pre- a hot environment. With body tempera-
venting excessive heat loss from the feet tures of 40°–42°C, birds are dangerously
during long periods of feeding (wading) close to their lethal body temperatures

227

1stPages_B.indd 227 7/22/20 11:35 AM

 of 44°–46°C; thus, birds can withstand ing blood flow to the feet. For example,
only a small amount of overheating Herring Gulls (Larus argentatus) can lose
before they die. Because of their small 80% of the heat generated in flapping
size, high metabolic rates, and large sur- flight through their feet. The amount
face-area-to-volume ratios, birds can heat of heat loss is no doubt aided by the
up as well as cool off very rapidly. In additional surface area of the webbing
addition, most birds are diurnal, which between their toes. The final morpholog-
exposes them to the direct heat of the ical adaptation we will consider, plum-
sun. Finally, most birds fly, which gener- age coloration, is rather difficult to gen-
ates heat at a rate about 9–12 times that eralize (as it was for dealing with cold
of basal metabolism. All these factors conditions). It might seem that white
mean that a bird living in a hot environ- plumage would be beneficial to heat loss
ment must be able to find ways of losing because of its higher reflection of visible
heat. Since environmental temperatures light energy, while black plumage would
are usually lower than bird body tem- be maladaptive because of its higher
peratures, birds can transfer heat to the absorbance of visible light energy. In
environment passively by radiation, con- fact, a bird with black plumage may be
duction, and convection. However, once able to use the plumage as a heat barrier,
environmental temperatures equal or by holding the feathers away from the
exceed body temperature, these routes of body and increasing the dead air space
heat transfer are unavailable, and evap- that insulates the skin from the feather
orative heat loss must compensate for surface temperature. While a black bird
both the internal heat produced and the in a generally bright desert environment
external heat load. Although it is difficult might seem vulnerable to predators,
to separate the effects of heat and water apparently it can hide rather easily in
stress when both involve evaporative the shadows generated under these light
heat and water loss, we will begin here conditions.
with a look at the ways in which birds A variety of behavioral adjustments
cope with high temperatures and then to heat are used in concert with plumage
look at how water is conserved in arid characteristics to offset heat gain. Birds
conditions. can orient at an angle to the wind that
As with cold, adaptations to extreme provides the maximum convective heat
heat utilize morphological, behavioral, loss. One study found that a black bird
and physiological adjustments. Morpho- that orients itself at a 160° angle from
logical adjustments to heat are generally direct sun exposure can become effec-
the opposite of those for cold conditions. tively white as far as radiation is con-
Birds in hot environments often have cerned.17 The postural changes exhibited
thin skin and feather layers and longer in response to heat stress are summa-
or larger extremities (head and legs) that rized by illustrations in figure 8.8.18 In
facilitate the dissipation of heat to the the absence of any heat load, incubating
chapter 8

environment. The exposed areas may Heermann’s Gulls (Larus heermanni)

have high concentrations of blood ves- present their minimum surface area by
sels near the surface to accelerate heat tucking in their extremities. As the heat
loss. A few species can cool by increas- load increases, the gulls elevate the scap-

228

1stPages_B.indd 228 7/22/20 11:35 AM

 Fig. 8.8. Postures exhibited by incubating defecate on their legs to gain the cooling
Heermann’s Gulls (Larus heermanni) in effects of evaporation.
response to increasing heat load (Bartholomew Physiological adaptations to mini-
and Dawson 1979). mize heat stress are generally the most
costly because some heat must actually
be generated in order to lose heat. The
ular feathers, increasing the convective heat is lost through evaporation of water
loss, and then extend the neck and open (560 cal/​mg water) from bare skin, by
the mouth (gaping) to facilitate both panting, or by gular flutter. Birds do not
convective and evaporative loss. Finally, sweat; they have no sweat glands and
gaping progresses to panting, and the the feathers would impede evaporation
body is tilted forward, exposing the from the skin in any case. Optimally,

Adaptations for Survival in Extreme Environments

shaded sides and flanks to convective a heat-stressed bird should increase
heat loss. the amount of evaporation at minimal
Of course, most birds do not have to cost, so that the evaporative heat lost
spend all their time in the sun. Instead, is greater than the heat generated by
they can forage during dawn and dusk evaporative cooling (evaporative water
hours and choose a cooler microenviron- loss to heat production ratio, EWL/​HP
ment during the heat of the day. In a few > 1). Panting, characterized by shallow
species, the nest is in particularly cool and rapid breathing, is one method of
locations and may even provide insula- increasing evaporative cooling. Gener-
tion from midday heat. Cavities also pro- ally, as body temperature rises, the pant-
vide protection from heat, and columnar ing rate also increases, and increased
cacti such as saguaro are noted for their evaporation occurs along the upper
cooling properties. A unique behavior respiratory tract. However, panting inter-
exhibited by a few species, such as vul- feres with normal respiration and tends
tures and storks, is urohydrosis. During to lower blood carbon dioxide levels and
periods of heat stress, individuals may raise blood pH.

229

1stPages_B.indd 229 7/22/20 11:36 AM

 A more efficient method that does
not affect respiratory gas exchange
or acid-base balance is gular flutter.
The gular area, which includes the
floor of the mouth, the throat, and the
anterior esophagus, can be manipu-
lated by muscles attached to the hyoid
apparatus. It is used by members of
many orders: caprimulgids, pelicans,
herons, cormorants, boobies, doves,
galliforms, and owls. The flutter rate is
much faster than that of panting, and
a larger surface area can be exposed
for evaporation. Temperatures of the
evaporative surface of the gular area
may be 5°C lower than core body tem-
perature (fig. 8.9). Although the rate of
panting usually increases with rising
body temperature, the hyoid apparatus
resonates at one particular frequency.
This feature reduces the effort added by
muscle contraction and consequently
reduces the heat production associated
with gular flutter. As a result, the gular
flutter rate is usually constant (except in
doves and pigeons). Occasionally, birds
may use both panting and gular flutter
to maximize their evaporative cooling.
For example, in the Brown Pelican (Pele-
canus occidentalis), the breathing rate
(panting) increases steeply with rising
body temperature, while the flutter rate
is constant.
As stated above, these methods of
achieving evaporative cooling are most
beneficial to the bird when the ratio of
evaporative water loss to heat production
is greater than unity (1.0). Passerine
birds can achieve an EWL/​HP ratio of
1.0 only by panting while breathing air
chapter 8

of low humidity, but other species can Fig. 8.9. Temperature of the head, neck, and
achieve ratios greater than 1.0 because gular regions of a cormorant during gular
of larger surface areas for evaporation, flutter (left) and posture of Great Cormorants
inherently low heat production rates, (Phalacrocorax carbo) during gular flutter.

230

1stPages_B.indd 230 7/22/20 11:36 AM

 or use of gular flutter. For example, the evaporative surfaces of the nasal pas-
the highest EWL/​HP ratio achieved by sages. This cooling mechanism enables
panting (1.8) was recorded from the birds to maintain more than a 1°C tem-
Papuan Frogmouth (Podargus papuensis), perature difference between the brain
which has an unusually large mouth. and the neck. The countercurrent heat
In comparison, one study measured an exchange in the rete is also important in
EWL/​HP ratio of 3.5 in a Common Poor- keeping the brain cool during flight.
will exposed to 47°C while the bird was
exhibiting gular flutter.19 The poorwill Adaptations to Xeric Conditions
also has unusually low basal metab-
olism, which greatly influences the The key to cooling off in hot environ-
magnitude of the ratio. This exceptional ments is water, but water is often limited
capacity of the poorwill to evaporatively in many arid areas or is available only
dissipate heat accounts for its ability to from saline pools. We must next con-
roost on the desert floor during daylight sider how birds cope with water depri-
hours in the summer. vation to maintain the proper water
Some birds can facilitate evapora- balance. While a few species fly long dis-
tive heat loss from the skin under heat tances daily to drink, most adaptations
stress, thus reducing the cost of cool- to limited water involve morphological
ing off. For example, at 30°C, 63% of or physiological adjustments, in which
the EWL from Chestnut-eared Finches water is obtained either from the diet or
(Taeniopygia castanotis) is via the skin. from saline water sources, or its loss is
Pigeons have a vascular plexus in the minimized by adaptations of the renal
neck that enables 60% of their evap- and excretory systems and by limiting
orative loss to occur across the skin at evaporation.
high temperatures (> 50°C).20 At these Water gain in xeric environments
temperatures, pigeons may stop panting can be achieved in several ways. One
and circulation to the periphery greatly source is the preformed water in food;

Adaptations for Survival in Extreme Environments

increases; presumably the bulk of the insects and vertebrates are about 60%–
evaporative heat loss is through the skin 75% water, and seeds contain about
at these extreme temperatures. 10% water. Metabolism of foodstuffs
When species are water or energy yields water in another way. For exam-
limited when exposed to heat, they ple, oxidation of 1 g of fat in food yields
may be able to survive brief periods of 1.07 g of water. Water formed as dew
hyperthermia, allowing their body tem- overnight can be scraped off the leaf or
perature to rise. When body temperature stem surfaces of plants during the early
exceeds environmental temperature, morning hours when the bird begins
birds can again transfer heat passively to forage. A rather special adaptation to
by radiation, convection, and conduc- water shortage is the transport of water
tion. A hyperthermic bird can still keep by sandgrouse (Pterocles spp.) and some
its brain cool because blood traveling species of shorebirds. Nesting adults fly
to the brain passes through a rete near long distances to water holes, soak their
the eye, where it is cooled by the venous breast feathers in the water, and bring it
blood coming from the beak area and back to the young. In some species the

231

1stPages_B.indd 231 7/22/20 11:36 AM

 Fig. 8.10. Salt gland of an albatross. nal or external nostril. A countercurrent
flow of blood in the capillaries and fluid
in the tubules (much like the counter-
breast feathers of the male are modified current system in the kidney nephrons)
to absorb water like a sponge. It has is very efficient in concentrating the
been estimated that sandgrouse can salt. For example, a gull given a quantity
carry up to 18 g of water 35 km using of seawater to drink equal to 1/10 of its
this technique. Some species can drink body weight can excrete almost 90%
saline water in xeric environments (or of the salt within three hours. The salty
seawater in marine environments) and fluid contains about 5% NaCl, compared
can then get rid of the excess salt either to seawater at 3% and plasma at 0.9%.21
through special salt-excreting nasal In many species, the salt gland can be
glands or by general adaptations of the inactive for months and then become
renal-intestinal system. active almost immediately following the
Salt glands are found in 13 orders consumption of seawater.
of birds but occur primarily in marine Water conservation is accomplished
birds; they also occur in terrestrial birds primarily through the actions of the
such as ostriches, raptors, some desert kidneys, chiefly through excretion of
species, and a few Arctic species that uric acid and by the tubular loops of
do not have access to fresh water. These Henle (similar to those in the mamma-
paired glands are situated in the skull lian kidney). Each molecule of uric acid
above or near the eyes (fig. 8.10). They eliminates twice as much nitrogen as a
are generally flat and crescent shaped molecule of urea, and the uric acid is rel-
and have many lobes. Each lobe has atively insoluble in water and much less
thousands of tubular glands surrounded toxic than urea or ammonia. To excrete 1
by blood capillaries, from which salt is g of uric acid uses only 1–3 ml of water,
chapter 8

removed and concentrated. The central compared to the 60 ml of water a mam-

duct of each lobe drains into a single mal uses to excrete 1 g of urea. The evo-
duct that empties into the nasal cavity lutionary significance of uric acid excre-
and out onto the beak at either the inter- tion is tied to oviparous reproduction in

232

1stPages_B.indd 232 7/22/20 11:36 AM

 birds. Avian embryos can develop in the a result of altered kidney function alone.
egg without dependence on exchang- In fact, the kidneys of many xerophilic
ing their nitrogenous wastes with the species do not demonstrate any obvi-
environment (as fishes, amphibians, and ous microstructural adaptations. Other
mammals do) by excreting the relatively mechanisms may be used to cope with
insoluble and nontoxic uric acid into an osmotic stress. Since uric acid is rather
allantoic depository. insoluble in water and tends to pre-
Renal tubular loops of Henle cipitate out in the urine as urate salts,
concentrate urinary waste by removing the collecting ducts and ureter secrete
water through a countercurrent multi- mucoid materials that help lubricate
plier system, just as in mammals, form- its passage and form colloidal suspen-
ing a urinary product that is about two to sions of the urate salts. When the salts
three times as concentrated as plasma. are removed from solution, the urine
Although hydrated birds may excrete is made less “salty” (hypotonic to the
as much as 33% of the water filtered blood), and this facilitates recovery of
by their kidneys, as little as 1% of the water in the cloaca. Urine entering the
filtered water is excreted by a dehydrated urodeum is mixed with feces in the
bird. This is about the same percentage coprodeum and passes back up the
of water recovery exhibited by mam- colon and into the caeca by the antiper-
mals. Water conservation by the avian istaltic waves of the colon. It is believed
kidney is aided by constriction of the that bacteria in the colon break down the
glomeruli of the reptilian-type nephrons, uric acid colloids and free some of the
which have no long loops of Henle (see salts, which are then reabsorbed along
chapter 2), and by increased permeabil- with water. More water reabsorption
ity of the tubules and collecting ducts to takes place in the caeca. Thus, recovery
water, under the influence of vasotocin of filtered water is not only accom-
(antidiuretic hormone) secreted by the plished in the kidney but is maximized
posterior pituitary gland. by reabsorption in the cloaca, colon, and

Adaptations for Survival in Extreme Environments

Generally, birds depend on fresh caeca of the bird.23 For example, a 2 kg
water, and only a few species are known chicken may filter 6 L of water a day: of
to survive on drinking water that is that, 5.5 L are reabsorbed in the kidney,
more concentrated than 50% seawater. 0.3 L is reabsorbed by the caeca, 0.1 L
In these few species, the ability of the by the colon and cloaca, and 0.1 L is
kidney to conserve water while handling excreted.
excessive sodium ions more nearly Under periods of unusual water
approaches the mammalian model. The stress when even the above solutions
best example of a bird that maximizes may not be adequate to ensure water
its renal salt-concentrating ability is the balance, birds have other safety valves
Savannah Sparrow (Passerculus sand- to which they can resort. Just as heat-
wichensis). These birds can drink seawa- stressed birds allow their body tem-
ter and form urine containing 969 mM perature to exceed a lethal level while
of sodium per liter; the urine osmolarity keeping the head cool, water-stressed
is then 4.5 times that of the plasma.22 birds may be able to withstand periods
Adaptation to xeric conditions is not of higher osmotic concentrations in

233

1stPages_B.indd 233 7/22/20 11:36 AM

 the plasma than normal. The Savan- behaviors in the titmice (Paridae) and
nah Sparrow, for example, can tolerate nuthatches (Sittidae).
serum concentrations as high as 610 Food storage is an attempt by a bird
milliosmoles per liter (normal values to save resources that are periodically
for birds are 300–350 mOsm/​L).24 superabundant for use when natural
Reduction of cutaneous evaporative loss availability of that resource is limited,
during dehydration and high ambient or weather conditions make search-
temperatures has been documented, ing for food difficult. The timescales
but the mechanism by which this is involved range from the storage of a
achieved is not well understood. Behav- daily excess for the next day to storage
ioral adjustments such as reduced systems lasting years. Many bird foods
activity and avoidance of high ambient do not lend themselves to storage for
temperatures help reduce respiratory long periods; fruits and insects decay
evaporative water loss. For example, the within a short time, as does the prey of
respiratory water loss of a Budgerigar carnivores. Only a few carnivore species
(Melopsittacus undulatus) during moder- have been observed storing prey for a
ate activity is 150 mg per hour, while at day or two. Noteworthy among these are
rest it is only 44 mg per hour.25 the shrikes (Laniidae), also known as
Using a combination of these butcher-birds for their habit of impaling
physiological, behavioral, and anatom- extra prey on thorns or barbed wire. In
ical adjustments to water restriction, contrast, seeds have basically evolved to
birds have successfully colonized xeric be dormant for some period, in many
environments. Several species, such as cases a year or more. This presents
the Black-throated Sparrow (Amphispiza many options for a foraging bird. On
bilineata) of the North American desert, a seasonal basis, seeds may be stored
have even become totally independent of in the fall for use in the winter, when
free water.26 they would be either in short supply or
inaccessible because of snow cover. Gray
Food Storage Jays (Perisoreus canadensis) stick seeds
to tree trunks with saliva, supposedly to
While many mammals take advantage keep them accessible following snowfall.
of seasonal resource variation by stor- These seeds are stuck high enough in
ing food for later use, this behavior was trees to be available above the snow that
thought to occur in only a few excep- accumulates through the winter. Acorn
tional species of birds. Recent studies, Woodpeckers (Melanerpes formicivorus)
however, have shown that some form store acorns and other seeds in small
of food storage occurs more commonly holes they have specially excavated for
in bird species, and new examples of this purpose (fig. 8.11). The birds then
species that store food are discovered use these “larders” or granaries to feed
each year. The classic cases of food themselves through the cold winter
chapter 8

storage occur in the Corvidae (crows, months and may also use them to feed
jays, magpies, and nutcrackers) and the the nestlings produced the following
Picidae (woodpeckers); recent work has summer. Less sophisticated storage
uncovered rather complex food-storage techniques employ natural cavities or

234

1stPages_B.indd 234 7/22/20 11:36 AM

 crannies and crevices in branches and
bark, while some species store seeds in
the ground.
Other species that store seeds may
be responding to even longer-term
variation in food supply. Some oaks and
pines produce seeds every two years or
so, but usually they then produce mas-
sive crops. Pinyon Jays (Gymnorhinus
cyanocephalus), nutcrackers (Nucifraga
spp.), and other food-storing species can
store large numbers of these food items.
Some have suggested that this interac-
tion is mutualistic, one in which both
species benefit. The birds serve the trees
as specially adapted seed dispersers that
bury seeds in favorable habitats and fail
to recover them all, while the trees pro-
vide the birds easy access to high-quality
food sources. The occurrence of peri-
ods of high resource availability (mast
years) ensures that there will be more
seeds than the seed eaters can eat, so
that many of the seeds will be stored
(buried) and not later recovered. The
alternative strategy of producing equal
numbers of seeds each year would likely
result in larger bird populations that
would harvest and eat a high proportion
of stored seeds. This would not result
in the seed dispersion favorable to the
tree. In the latter case, the bird would be
considered a seed predator, as it would
be destroying all the seeds. Only if more
seeds are dispersed than recovered does
the relationship constitute mutualism.
One of the best studied of these
interactions between a seed-eating Fig. 8.11. An Acorn Woodpecker (Melanerpes
bird and a seed-producing tree is that formicivorus) storing an acorn in one of its
between the Clark’s Nutcracker (Nuci- larder trees, where it drills holes specifically for
fraga columbiana) and the Pinyon Pine acorn storage.
(Pinus edulis) (table 8.2; fig. 8.12).27 In
this case, many characteristics of both
bird and tree suggest a mutualistic

235

1stPages_B.indd 235 7/22/20 11:37 AM

 Fig. 8.12. A Clark’s Nutcracker (Nucifraga ensures maximum dispersal. As stated
columbiana), one of several corvids that store above, though, these periods of seed pro-
seeds and are involved in mutualisms with pine duction occur only every few years; in
trees. the Pinyon Pine it appears that bumper
crops appear every six years, with some-
what smaller crops in intervening years.
relationship. The pine produces seeds What does the Pinyon Pine get in
that are large but not winged (thus they return? It has been estimated that a typ-
cannot be easily wind dispersed), have ical Clark’s Nutcracker will cache (store)
rather thin seed coats, and are displayed 22,000–33,000 Pinyon Pine seeds
in upright cones without sharp scales (in during the production of a seed crop. Yet
contrast to most pines, where the seeds each nutcracker needs to recover only
are protected within scaly cones that about 850 of these to survive through a
hang downward to aid in wind disper- typical winter. Quite obviously, the pine
sal). Pinyon Pine seeds are relatively is getting a vast number of seeds dis-
large, which attracts the birds, and persed and planted by the nutcrackers.
fertile seeds are readily distinguished For doing all this work, the nut-
from infertile seeds (which increases cracker has access to a very nutritious
the seed disperser’s efficiency). While food that many species cannot harvest.
chapter 8

wind-dispersed pine seeds are usually As long as it can remember where it

all released at once to reduce the effects has hidden the seeds, it has easy access
of seed predators, Pinyon Pines release to food for a long period. This food is
their seeds over several months, which nutritious enough that it allows the

236

1stPages_B.indd 236 7/22/20 11:37 AM

 Table 8.2
Characteristics of bird and pine that favor a mutualistic system such as that of the
Clark’s Nutcracker and Pinyon Pine, compared to birds and trees with more typical
seed predator systems
eat seed for cache seed for
­immediate energy later use
bird
Size Small Large
Energy state Negative to neutral Positive
Relative longevity Short Long
Residence status Migratory-transient Permanent
Ability to find hidden food Poor Good
environment

Predictability High Low

Harshness Mild Severe
seed

Amount Rare Abundant

Ease of obtaining Difficult Easy
Ease of concealing Difficult Easy
Size Small Large
Permanence of uncached food High Low
Permanence of cached food Perishable Stable
Source: Balda, 1980.

nutcrackers to breed early in the spring, items in locations where they would be

Adaptations for Survival in Extreme Environments

before other foods are available. It is found through normal foraging later on.
also nutritious enough that it makes up Storage, therefore, did not involve any
a substantial proportion of the diet fed great capacity for memorizing locations.
to the young, an unusual trait among Recent studies, however, show that
seed-eating species. Pinyon Jays will birds have a highly developed capacity
breed in the autumn during seed crop to remember exact locations where
years, apparently cued by the presence they have stored food items. Laboratory
of green seed cones. experiments with jays and nutcrackers
For food storage to be successful, show that they can remember a large
the bird must be able to remember number of exact locations for many
where it has put the food. Recent studies months.28 In these experiments, jays
have examined the ability of birds to and nutcrackers stored seeds in a special
remember where they have stored food grid of sand-filled cups within a labo-
items. Early workers thought that birds ratory room and then were kept away
did not recall particular storage sites, but from that room for a lengthy period.
that food storage involved placing food When birds were released to find this

237

1stPages_B.indd 237 7/22/20 11:37 AM

 food, they did amazingly well, even after food shortages. When the breeding
several months. Graduate students pre- season comes, though, only a few birds
sented with the same situation did much breed at a single nest. As we will discuss
more poorly than the birds! In studies in somewhat more detail in chapter
of wild chickadees, observers watched 12, this may be a monogamous pair, or
individuals store food items and then a group with two of one sex and one
moved them. In many cases, a bird did of the other. Other birds in the group
not find a food item moved just a few help with the breeding but do not breed
inches, presumably because it had such themselves. This unusual social system
an exact recall of where the seed was seems to revolve around the constraints
stored. These studies have suggested put on this species by its system of food
that a chickadee may be able to recall storage and the long time required to
up to 300 exact locations where it has make the holes to store food.
stored seeds. Many examples of birds that store
We have already suggested that food have been discovered in recent
patchily abundant food supplies often years, and more will likely appear. The
favor group foraging. Such is often the form of storage varies with the foods
case with seed-bearing trees, and food available and the characteristics of the
storage may enhance this tendency birds involved. Long-term mutualisms,
toward sociality. This is particularly such as that of the Pinyon Pine and
true when the food is stored in a special nutcracker, require birds that live long
location, as in the granary trees of Acorn enough to respond to long-term food
Woodpeckers. Several of the jay species cycling. Jays and nutcrackers are large
associated with mast crops have unusual and sufficiently long-lived to be able
group-breeding social systems, which is to adapt to multiyear cycles. Smaller
due at least partly to this interaction with species like chickadees often do not
their food supply. Pinyon Jays are able live long enough to adapt to such long
to feed their young Pinyon Pine seeds. cycles; for these species, we may find
Groups store seeds and then recover that seed storage is purely an adaptation
them later to feed themselves or their of a seed predator taking advantage of a
young. Young birds may face a decision seasonally abundant resource. Plant-an-
early in life that favors staying with imal mutualisms of the sort discussed
the group so that they have a chance to above should be rare, as should the
share group-stored food and thus sur- occurrence of group-breeding social
vive, even if that means not breeding for systems revolving around food storage.
several years. Even though food storage is rare,
Perhaps the most unusual social sys- it exemplifies the range of adaptations
tem found among food-storing species birds have evolved to survive in harsh
is that of the Acorn Woodpecker. The and seasonal environments. Next, we
granary trees mentioned above (fig. 8.11) will look at those species that appar-
chapter 8

are often guarded and provisioned by a ently cannot adjust to a single location
group of up to 15 birds. These birds all through the whole year and have evolved
help ensure that food is saved when it is migratory behavior.
available, and all are able to use it during

238

1stPages_B.indd 238 7/22/20 11:37 AM

 C HAP T E R 9

Migration

A
lthough birds have a wide “for most communities, we must be
variety of adaptations that genuinely puzzled by all the comings
allow them to survive harsh and goings.”
conditions, these sometimes In this chapter we hope to describe
are not enough and the best long-term and explain some of these comings and
strategy for a bird is to leave the area goings, along with the various mech-
in which it has been living. Virtually anisms of navigation and orientation
all such movements have been called required to accomplish them. We begin
migration, although as we will see, a with a look at the terms used to describe
wide variety of movements occur in various types of migration and then
the bird world. Most everyone who look rather extensively at which species
has lived in the temperate zone is well migrate and at the general patterns
aware of migration through the obvious of their travel. The very complex and
seasonal movements of flocks of geese sometimes nearly incredible adaptations
or blackbirds. It takes no genius to see that birds use to get between wintering
how the deep snows and cold tempera- and breeding grounds are discussed
tures of winter may force many species next, followed by a look at modern ideas
south, but migration is a much more behind the evolution of migratory behav-
complex phenomenon than simply ior in birds. The model presented, like
forced movement. The subtle seasonality most evolutionary models dealing with
of most tropical habitats leads to the complex phenomena, evaluates various
migration of some species away from trade-offs available to migrant or resi-
habitats where some north-­temperate dent individuals in an attempt to offer
breeding birds spend the winter. Why insight into the evolution of all migra-
do some of these move, while the tory behavior.
“invaders” from the north do not?
Given that these northern breeders can Definitions of Movements in Birds
survive for up to nine months a year on
the “wintering” grounds, why do they The term “migration” may be used to
leave at all? Many examples exist where cover any movement of birds, including
a breeding species flies south for the travel in nearly all directions at nearly all
winter but is replaced in its breeding times of the year, with or without return
range by a wintering species that seems trips. Our lack of understanding of the
nearly identical to it in overall ecology. details of migration often reflects the
Why doesn’t one species just stay put? insufficient data we have on character-
As Steve Fretwell suggested in 1980, istics of avian populations. For example,

239

1stPages_B.indd 239 7/22/20 11:37 AM

 we may see individuals of a species in when their food supply is low in their
a habitat all year long, but are they the normal wintering habitats, resulting in
same individuals, or are changes occur- sometimes impressive invasions into
ring as individuals replace each other areas where these species are normally
sequentially? absent or uncommon. A number of
In its purest sense, migration refers northern seed eaters such as crossbills
to seasonal movements between a loca- and grosbeaks show these movements,
tion where an individual or population apparently when the northern conifers
breeds and a location where it survives produce few seeds. Raptors that special-
during the nonbreeding period, usually ize in such cyclic prey as lemmings also
the winter. Long-distance migrants are may show irruptive movements, while
those that have a complete shift between in the tropics certain bamboo specialists
breeding and wintering areas, such as show invasive movements that follow
the Blackpoll Warbler (Setophaga striata), the infrequent production of seeds by
which breeds in boreal forests of Can- bamboo plants.
ada and Alaska but winters in northern Other terms associated with migra-
South America (fig. 9.1a). Short-distance tion distinguish winter, summer, and
migrants make shorter trips, perhaps permanent residents. Winter residents
only up and down a mountain slope are species that spend the winter in a
with the changing of seasons; breeding particular area, whereas summer resi-
and wintering ranges may overlap, as in dents are those that spend the summer
the Pine Warbler (Setophaga pinus; fig. and usually breed there. Permanent
9.1b). Partial migrants are those popula- residents are species that occur in a
tions in which some individuals migrate location all year, although in many cases
but others remain for the harsh period. individuals may migrate so that there
As we will see, this variation may be are both winter resident and summer
related to age and sex of individuals, or resident populations of a permanent
it may be directly tied to climatic factors. resident species. These terms unfortu-
Not surprisingly, a species with a broad nately reflect the pervasive temperate
range may have individuals or popula- bias in field biology, particularly when
tions that exhibit all of the above types of they are applied to birds that spend long
migration. periods (up to nine months) in the trop-
Many species have movements that ics. Can we speak of “winter residents”
are less regular but are nonetheless in a tropical land that has no winter? In
forms of migration. “Dispersal” is the some tropical areas, nonbreeding birds
term given to unidirectional movements from temperate zones may not migrate,
from one location to another. These such that “winter residents” are present
are most often done by young birds all year long. While we must keep these
as they leave their natal territory and problems in mind, these terms are a
search for a breeding place of their own. part of the ornithological literature and
Irruptive or invasive movements may are convenient when dealing with tem-
chapter 9

involve back and forth travel, but they perate zone situations.
also often involve wandering. Species Another set of terms associated with
show irruptive movements during years migration has to do with the exactness

240

1stPages_B.indd 240 7/22/20 11:37 AM

 a

Fig. 9.1. (a) Long-distance and (b) short- the Atlantic Ocean in the fall and an overland
distance migration in two warblers. The route in the spring. Pine Warblers (b; S. pinus)
Blackpoll Warbler (a; Setophaga striata) in the southern part of their range are residents
has widely separated breeding and wintering all year, while more-northern breeders make
grounds, with a complex movement pattern short trips between wintering and breeding
that includes a two- to three-day flight over ranges.

1stPages_B.indd 241 7/22/20 11:37 AM

 b

1stPages_B.indd 242 7/22/20 11:38 AM

 of movement by individuals. Many each winter, Northern Parulas (Seto-
species show patterns where individu- phaga americana) seem more nomadic.
als spend both winter and summer in This species is seen regularly, but we
specific locations, perhaps returning have only one recapture out of dozens
to exactly the same territory in two banded. Yet this recapture occurred after
different areas. This trait is known as seven years, so perhaps the Northern
site faithfulness or site fidelity. While Parula shows a general site faithful-
it has long been known that this trait ness (say to the forests of southwestern
existed among birds returning to breed- Puerto Rico), but nomadic behavior on a
ing grounds, recent work has shown more local scale.
that many species also return to exact Although most migrants generally
locations on their wintering areas. The migrate between two locations, in some
author has recaptured the same Amer- species there may be three or more areas
ican Redstart (Setophaga ruticilla) at the involved. Many waterfowl that undergo
same location in Puerto Rico over an flightless periods during molt under-
11-year period; other researchers have take special flights to areas particularly
recaptured redstarts on the same breed- well suited for molting. These molt
ing area for nearly as long. migrations may take a bird to lakes with
A special case of site fidelity is plentiful food and few predators. In Can-
termed philopatry. This refers to birds vasbacks (Aythya valisineria) that breed
that return to the location where they on the northern prairies of the United
were born, so the term has a breed- States, this molt migration is north-
ing-season bias. Characteristics of site ward to the prairie provinces of Canada.
faithfulness or philopatry may vary Many songbirds of the western United
between the sexes. In most passerines, States and Canada leave their breeding
males are often more philopatric than grounds in midsummer after breed-
females. In species such as ducks, pairs ing. They head to southern Arizona
often form on the wintering grounds. In and ​New Mexico and to northwestern
this case, the female returns to its natal Mexico, where late summer monsoonal
area while the male simply goes where rains result in lots of plant growth that
its female mate goes. The mechanisms provides food to promote the annual
of site fidelity or philopatry will be exam- molt (although some of these birds may
ined later. In contrast to these rather also produce a second brood of young
specific movements, the movements of after this movement; fig. 9.2).1 After
some species are much more nomadic. molting, these birds then move to their
These may head for a general area but wintering grounds for the remainder of
do not seem to return to specific sites as the nonbreeding season. Other species
the species discussed above do. Varying apparently require multiple locations
degrees of site faithfulness or nomadism to have enough food to survive through
undoubtedly occur. For example, in the the year. Many hummingbirds fit this
same location in Puerto Rico where we pattern; Anna’s Hummingbirds (Calypte
Migration

find that American Redstarts and Black- anna) breed in the coastal chaparral of
and-white Warblers (Mniotilta varia) southern California, summer in the high
regularly return to the same location mountains of California, and winter

243

1stPages_B.indd 243 7/22/20 11:38 AM

 Fig. 9.2. Migrational movements of two
populations of the Painted Bunting (Passerina
ciris). Birds that breed along the southeastern
coast winter in southern Florida and the
western Greater Antilles and have simple
movements between these areas. Birds with
a breeding range in the south-central United
States do a molt migration to the Desert
Southwest and then move to their wintering
range in Mexico and Central America.

1stPages_B.indd 244 7/22/20 11:39 AM

 in the deserts of Arizona and Mexico. and accessibility of food. For example,
Western Kingbirds (Tyrannus verticalis) fish spend the winter in a lake, but if that
appear to move through most of the lake is ice covered, they are inaccessible
nonbreeding season in their Mexican to birds. Let us briefly consider the food
wintering grounds, staying in the same and ​foraging groups discussed in earlier
location for only a few weeks at a time.2 chapters, thinking about the options each
While the above terms are intended has in response to seasonal variation in
to help categorize migrant species, its food supply, emphasizing, for now, the
migration is obviously complex. Our temperate zone.
difficulties in understanding it are Most temperate birds feed on
compounded in many cases by our lack insects, especially during the breeding
of information on the specific traits of season, but this food is very limited
many migrant species. Recent work has in availability during the cold winter
helped consolidate our understanding months. Terrestrial insects are not active
of migratory behavior (see below), but during cold weather, and the seasonal
much of this work has also accented the nature of many temperate habitats fur-
many strategies migrant birds use to ther limits the insects’ growing season.
survive the annual cycle. Those insects that overwinter as pupae
or adults decline in number during the
Which Species Migrate and winter as foraging birds find these food
Where Do They Go items. Not surprisingly, insect eaters
Food habits and migration are the largest group of migrants (fig.
9.3).3 Only a few species classified as
In chapter 8, we saw that many species of insect gleaners winter in cold temperate
birds can survive almost any weather con- environments. These feed on insects
dition if they have enough food. There- to some extent, but they also add seeds
fore, it is not surprising that food habits to their diet (as does the Black-capped
are closely related to migratory behavior
in birds. In looking at the relationship Fig. 9.3. Food habits of North American
between food habits and migration, we migrants (Rappole, Morton, Lovejoy, and Ruos
must keep in mind both the existence 1983).
Migration

245

1stPages_B.indd 245 7/22/20 11:39 AM

 Chickadee [Poecile atricapilla], discussed limitations in the North Temperate
in chapter 8). Wintering insectivores in Zone and most must travel southward
Northern Hemisphere forests include to some extent. These may not have to
many members of the Paridae, which travel all the way to the tropics, though,
have much heavier bills than most insec- as the more moderate climates of the
tivores, a trait that allows them to feed southern United States may produce
on seeds and other hard materials. The enough food for them to survive the
warbler groups of the northern conti- less harsh winter conditions. Thus, we
nents (Parulidae and Sylviidae) have see many of the thrushes and robins
thin, sharp bills that limit them to feed- wintering in the southern parts of the
ing almost exclusively on insects and North Temperate Zone. In contrast to
may force them to migrate when insects fruits, seeds are made to last the winter
are limited in availability. Because of the and may remain available throughout
potentially devastating effects of rare that period. Of course, no new seeds are
insect shortages caused by cold weather, produced during the winter, so resource
most insect gleaners travel far to the depletion is possible, and snow cover
south to spend the winter. may make many seeds inaccessible. In
Because few insects fly during cold general, though, seed eaters can winter
weather, aerial insectivores are forced much farther north than most other
to migrate, as are nearly all fly-catching small birds. Species such as crossbills
insectivores. A few flycatchers (such as and finches that feed on pinecones or
the North American phoebes [Sayornis]) other aerial seed supplies do not even
may winter in the southernmost parts of have to deal with snow cover. Those
the North Temperate Zone, particularly seed eaters that must move southward
along watercourses where some insects generally do not travel great distances.
emerge throughout the winter months. While this may reflect adequate seed
Aquatic insectivores face reductions in supplies in the southern parts of the
food availability because of ice cover; North Temperate Zone, it should also be
most species winter in the tropics or noted that most tropical forests produce
even move to the South Temperate Zone fruits rather than simple seeds, so the
during its summer. A few remain along tropics may not be a viable option as a
ocean shorelines as far north as ice-free wintering ground for many seed eaters.
conditions will allow. In general, fish-eating waterbirds
Fruit- and seed-eating species face can survive as long as the bodies of
markedly different conditions in the water on which they stay do not freeze
temperate zone. Both resources are over. Thus, we see that the winter ranges
produced in great quantities during of many of these species are limited
the temperate zone summer, but their by ice-free conditions in the interior of
availability during the winter differs continents but may extend far to the
sharply. Fruits are generally available for north along coastlines. Some wintering
only a few weeks during the summer waterfowl literally follow the movement
chapter 9

or early fall; only a few plants have soft of ice through the winter, flying south a
fruits that remain into the winter. As few hundred miles when it gets cold and
such, true fruit eaters face rather sharp then moving northward during thaws.

246

1stPages_B.indd 246 7/22/20 11:39 AM

 Of course, the actual diet of waterbirds to migrate from the north much more
affects their movements above and than owls, which actually benefit in terms
beyond the presence of open water. of foraging time from the effects of the
Species that feed on insects or vegeta- long winter night. While many migrant
ble matter may be forced farther south raptors winter in the southern parts of
because of a decline in productivity the North Temperate Zone, a few travel
during the cold months, and the pres- to the tropics or even beyond. For exam-
ence of large concentrations of migrants ple, Swainson’s Hawks (Buteo swainsonii)
in limited coastal areas may force some leave the grasslands of the western
species to travel farther than the occur- United States and Canada to spend the
rence of resources alone might suggest. winter on the grasslands of Argentina.
While most aquatic birds winter in the Nectarivores may be the group most
southern portions of the temperate obviously limited by cold conditions.
zone, a few enter the tropics and some Few plants bloom during the winter, so
even migrate to the Southern Hemi- the few nectarivores found in temperate
sphere. Particularly well known among zones during the summer must head
these is the Arctic Tern (Sterna arctica), south in the autumn. A few species,
whose migration takes it from the east- however, do winter in southern parts of
ern coast of Canada to the Antarctic and the North Temperate Zone, particularly
back during each winter, a round trip of in arid regions where rains during the
about 35,000 km. The most impressive winter months cause the blooming of
record for long-distance migration in many flowers.
a single jump is that of the Bar-tailed While the above brief analysis pro-
Godwit (Limosa lapponica), which breeds vides an idea about which types of birds
on the Arctic tundra, stages in coastal face strong resource limitation during
Alaska, and then flies to New Zealand the winter, resource limitation is just
for the winter. Sometimes individuals one of the factors with which a species
will fly nonstop for 10,000 km, from must deal. Before a migrant can be
Alaska to New Zealand.4 successful, it must have a nonbreeding
Raptors also face seasonal food area with sufficient food, a factor that
limitations, depending on their specific reflects both climatic conditions and
food supply. Species that feed on rodents the presence and abundance of other
may not face drastic declines in rodent species feeding on that food. With the
numbers, but snow cover may affect above generalizations in mind, let’s look
the accessibility of this prey. Bird eaters at some of the problems of geography
must deal with the migratory nature and habitat distribution that migratory
of many of their potential prey items, birds may face.
while insect-eating raptors face the same
problems as other insectivores. In the The effects of geography and
Far North, raptors not only face problems habitat on migratory behavior
with prey densities but must deal with
Migration

very short daylight periods during the The preceding section identified the
winter. Perhaps it is not surprising that types of species that might face prob-
hawks, which forage during the day, tend lems surviving on their breeding

247

1stPages_B.indd 247 7/22/20 11:39 AM

 some rather striking asymmetries in the
arrangement of the world’s land areas.
Generally, there is more land area in
the North Temperate Zone than there
is in either the tropics or the South
Temperate Zone—in other words, more
breeding area than potential wintering
grounds for temperate-breeding birds
(fig. 9.4). If we look at the dominant
habitat types in these areas, the con-
trast is even sharper. For example, in
the Western Hemisphere, the total area
of tropical forest in South and Central
America may equal the amount of forest
in North America, but there is a very
limited amount of other habitat types in
the tropical zones (fig. 9.5).5 Grassland
species attempting to winter to the south
must either stop in the southwestern
United States or northern Mexico or
fly all the way to the Llanos of Venezu-
ela or the Pampas of Argentina. Only
very limited areas of grasslands exist
between these areas. Wetland species
of the vast Arctic tundra find nothing
comparable in much of South America.
These species either spend the winter
on the coasts or travel all the way to the
grasslands of Argentina. Although the
amounts of forest in North and South
America may be roughly similar, we
Fig. 9.4. Simplified distribution of habitat types must remember that in the temperate
in the New World, showing tundra, desert,
zone these include conifer and decid-
grassland, temperate forest, and tropical forest.
uous forests, whereas tropical forests
range from rainforest through a variety
grounds through the winter. For all of very seasonally dry scrub forests.
of these to move south, there must be Migrants must deal with these differ-
enough area to support them, includ- ences in forest type, even if the quantity
ing not only enough land or water area, of forest is approximately the same.
but the proper habitats and sufficient The situation in the Old World may
resources for them to survive alongside be even more asymmetrical in terms of
chapter 9

the species that spend their whole lives habitat similarity between the winter-
in these more southerly areas. ing and breeding grounds. Once again,
A quick look at a world map shows there is a much greater land area in the

248

1stPages_B.indd 248 7/22/20 11:40 AM

 temperate zone than in the tropics, but
much of this tropical land is covered
by deserts, arid thorn scrub, savannas,
or high mountains. Tropical and sub-
tropical forests are limited to equatorial
Africa, parts of the Indian peninsula,
and much of Southeast Asia and its
nearby islands. Whereas the habitable
area of Africa is similar to that of the
Neotropics, India is only about 20%
this size, and Southeast Asia about
10%. This contrasts with the vast areas
of temperate deciduous and coniferous
forest in the Old World, an imbalance
that must have been dealt with in the
evolution of migration. It is also import-
ant to note the major barriers that exist
between potential breeding areas and
the best wintering grounds (i.e., the
Mediterranean Sea and the Sahara Des-
ert in Africa, and a variety of deserts and
mountains across southern Asia).
This lack of balance in potential win-
tering and breeding habitats is another
problem that affects the occurrence of
migration in birds. While birds show
great flexibility in behavior that allows
them to use very different habitats or
foods on the breeding grounds com-
pared to wintering areas (fig. 9.6), there Fig. 9.5. Equal-area projection of North and
are limits to this flexibility. Thus, it is South America, where the latter has been
hard to imagine a sandpiper foraging on rotated to show relative amounts of land area
the floor of a rainforest, or a Swainson’s in temperate and tropical zones. The same
Hawk trying to survive in tropical scrub. could be done for the Old World (Myers 1980).
In addition, the effects of the great
number of species that stay put must be
considered, for they, too, affect whether within and among species, it is difficult
a particular area is a viable location for a to say that “this region has this many
migrant to spend the winter. migrants and this many residents.” We
just do not know enough about which
General patterns of movement species move and which do not to make
Migration

this determination for all but a few

Which species leave? Because of all the sites. Even when we know that a species
variation in how migration occurs both moves from one site to the next, if that

249

1stPages_B.indd 249 7/22/20 11:40 AM

 species has a fairly broad range on both Fig. 9.6. General distribution of habitat use by
its breeding and wintering grounds, we North American species that migrate to the
generally do not know whether local tropics in winter (Rappole, Morton, Lovejoy,
breeding populations have specific win- and Ruos 1983).
tering sites and so forth. We will discuss
this problem a bit more at the end of Neotropical migrants (those that winter
this chapter when we discuss conser- in truly tropical areas; fig. 9.7). Within
vation of migrants. Until then, we can the grassland samples, they found
look at general patterns of movement that the tendency to migrate ranged
from various habitat types in the tem- from 100% in some of the most north-
perate zone and patterns of occurrence erly sites to less than 60% in Texas.
of winter residents in the tropics and A relatively small percentage of these
subtropics. grassland species winter in Neotropical
In North America, researchers have areas, presumably because of the habitat
tried to estimate the extent of migration limitations mentioned earlier. Most
in several north-temperate habitats by remain in the southern portions of this
utilizing breeding censuses done by grassland region for the winter.
amateurs under the supervision of the The northern coniferous forests
National Audubon Society.6 Using 40 of face severe winter weather, so it is not
these censuses from three major habitat surprising that between 80% and 100%
types in North America, these authors (average 94%) of individuals and 50%–
were able to compute both the per- 100% of species that breed in these hab-
chapter 9

centage of species and individuals that itats migrate. Approximately two-thirds

migrate from this region and the pro- of these migrants (including a great
portion of these that can be classified as many Parulidae) migrate to the Neo-

250

1stPages_B.indd 250 7/22/20 11:40 AM

 Figure 9.7. Proportions of individuals that tropics, while the remainder stay in more
migrate from North American breeding sites southerly deciduous forests. That these
to tropical locations. Red sectors of circles deciduous forests are somewhat less
denote these tropical migrants, while white severe in winter is suggested not only by
sectors signify both resident and short-distance the occurrence of these coniferous forest
migrants. Green represents the forested zone breeders in winter, but by the fact that
(MacArthur 1959; Willson 1976).
only about 75% of breeding individuals
and 62% of breeding species migrate
from them. While the deciduous forest
is apparently so different from summer
to winter, a large amount of bark surface
Migration

is available all year and the climate is

generally milder, with less snow cover
than is found in coniferous habitats. The

251

1stPages_B.indd 251 7/22/20 11:41 AM

 latter fact may allow the survival of many waterbird migrations from east to west,
ground-dwelling seed eaters. between the very seasonal lakes and
Formal examinations of migration ponds of temperate eastern Europe and
among other temperate birds of the New Asia and the coastal marshes of western
World have not been published, but Europe.
many patterns are obvious. We know Not surprisingly, given its rather
that none of the breeding sandpipers of isolated location, Australia has few
the Arctic tundra spend the winter there, migratory birds. It has been estimated
and virtually all the waterbirds of the that only 8% of Australia’s species show
interior marshes and lakes also migrate. north-south migrations. In contrast,
While this leaves a general picture of 26% show nomadic movements, appar-
mass exodus from northern habitats, the ently because of the rather harsh and
situation in the southern part of the tem- irregular aridity of much of interior
perate zone is very complex, with both Australia.
breeders that winter to the south and
winter residents that breed to the north. Where do they go?
Somewhat different types of analy-
ses have been done on Palearctic com- Some of the limitations that determine
munities, but similar results have been where some species can spend the
obtained. It has been suggested that winter have already been suggested.
about 40% of the species of that region Waterbirds that breed in the north must
leave it completely for the winter and use either southern lakes or oceanic hab-
go to either Africa or the Orient.7 The itats. Grassland birds are constrained by
Old World temperate zone is dominated the limited distribution of grasslands in
by coniferous forest, the habitat with tropical areas.
the highest rates of migration in the At least in the New World, forest
New World, plus large areas of decidu- species do not seem to be as constrained
ous or mixed forest and relatively little by the available area of acceptable
grassland. Researchers used a variety of habitat. The large area of temperate
censuses and extrapolated to total hab- forests suitable for breeding seems to
itat area to estimate that this migration be matched by the extensive forests of
totaled five billion birds moving out of South America plus sizable tracts of
Old World habitats each fall. forest in Central America. Surprisingly,
Waterbirds in the Old World face however, recent studies have shown that
many of the same limitations as in the the vast tropical forests of the Amazon
New World, but some climatic differ- basin are little used by North American
ences between these regions affect breeding birds. Nearly all these migra-
migration patterns. Because of the Gulf tory species spend the winter in Central
Stream, much of western Europe has a America, the West Indies, or montane
fairly mild winter climate that allows the habitats in northern South America. Rel-
survival of coastal wintering forms in atively few of these forest species enter
chapter 9

large numbers. This, coupled with the the vast forests of Amazonia, and these
limited availability of suitable habitat generally occur in very low densities
to the south, leads to many Palearctic relative to residents.

252

1stPages_B.indd 252 7/22/20 11:41 AM

 A closer look at some of the largest support few migrant species, although
migratory groups shows this general pat- those of Southeast Asia support large
tern quite clearly.8 The small New World numbers of migrants.
warblers (Parulidae) are among the most
diverse of migrant groups. Species and Age and sex differences in migrants
individual densities of these warblers
are highest in southern Mexico, Central To add to this complexity of migrant
America, and the West Indies. Very few behavior, many species show differences
winter in northern South America. Fly- between the sexes and/​or between adults
catchers of the family Tyrannidae show a and young birds in patterns of migra-
similar pattern in Mexico and in Central tion. In most cases where the sexes
and South America (fig. 9.8),9 but very have different wintering areas, males
few winter in the West Indies. Other stay farther north than females. At least
insectivores, such as swallows, swifts, three hypotheses have been offered to
and vireos, also winter primarily in explain this pattern.10 The arrival-time
this region, as do migratory humming- hypothesis suggests that since males
birds and those migratory finches and need to return to their breeding grounds
sparrows that go farther south than the to compete for territories as early as
United States. It is quite obvious that this possible in the spring, males stay as
relatively limited area of Central America far north as they can survive. Females,
supports the bulk of migratory North without as much pressure to get back
American breeding birds (fig. 9.9). to the breeding area, can winter far-
In the Old World, a quite different ther south, presumably where life is a
set of patterns occurs. Much of Africa little easier. The body-size hypothesis
is covered with savanna or other open suggests that the larger males can stay
forests, and these habitats support most farther north because they have a more
of the migrants. Rainforests of Africa favorable surface-area-to-volume ratio

Fig. 9.8. Distribution of resident

and migrant species of flycatchers
(Tyrannidae) on New World
wintering sites. Note that few
flycatchers go as far as South
America (Ketterson and Nolan
1976).

253

1stPages_B.indd 253 7/22/20 11:41 AM

 Fig. 9.9. Map showing the percentage of North
American migrant species wintering from
Mexico through Central and South America
(Rappole, Morton, Lovejoy, and Ruos 1983).

1stPages_B.indd 254 7/22/20 11:41 AM

 than females (as males are usually Dark-eyed Juncos (Junco hyemalis) show
larger than females). Support for this differences between males and females
hypothesis comes from many raptors, in wintering grounds (fig. 9.10), but
where the females are larger and may since the males also return to the breed-
winter farther north than males. The ing grounds before females, are larger
dominance hypothesis suggests that the than females, and are dominant in
dominant sex (also usually the larger male-female encounters, separating out
sex) forces the subordinate sex to move all the possibilities is a problem. Species
farther south. In this situation, the sub- such as the Spotted Sandpiper (Actitis
ordinate sex appears to face high mor- macularia), in which the female is larger
tality rates when attempting to coexist and returns first, are also difficult to
with the dominant under conditions of categorize, since in this case the female
food limitation; moving south increases is polyandrous and may be returning
the survivorship of individuals of the ahead of the male because it must
subordinate sex. compete with other females for space,
The problem with these hypotheses just as is the case for most monoga-
is that specific situations often fulfill mous or polygynous males. Raptors
the predictions of two or even all three.11 are also unusual in that females may

Fig. 9.10. Clinal variation

in the sex ratio of the
Dark-eyed Junco (Junco
hyemalis), showing the
percentage of females
in populations (Ruppell
1944).

Migration

255

1stPages_B.indd 255 7/22/20 11:41 AM

 be dominant in social encounters, so it genetically fixed ability to respond to the
is difficult to identify the critical factor, cues needed to return to the proper loca-
although researchers have developed a tion. In the case of philopatric individu-
model that considers all these factors als, the cues necessary for such homing
in the evolution of sexual differences in may be learned while the juvenile lives
migration. in its natal area before leaving in the
Differences in migration between fall, or they may be carried genetically.
age groups of birds may revolve around In either case, the problem then is to
the same set of factors as sexual differ- understand the orientation and naviga-
ences. In many of those species with tion abilities required to return to this
sex-related wintering range differences, exact location (see below).
young males winter in the same areas as Many other species show some flexi-
adult females for their first winter. The bility in selecting the areas to which they
arrival-time hypothesis would explain will return, at least early in their lives. In
this by the observation that young males these cases, it appears that a general set
have little chance of winning breeding of behavioral responses may be geneti-
territories when competing with older cally programmed such that they guide
males, so they are better off flying far- a young bird to a region. For example,
ther south their first winter and increas- a young American Redstart may carry
ing their chances of survival. During the genetic information that causes it to
second and subsequent winters, these respond to cues that guide it to Puerto
males remain farther north with the Rico, or perhaps just to the West Indies
other, more experienced males so that (we do not know how specific these may
they have a better chance of getting back be). This young bird may then spend
to their territories first. (We discussed the winter moving about, searching for
the advantages of site dominance in a good place to stay. Once settled on a
chapter 8.) The body-size or dominance site, it may stay in that area until it is
hypotheses would suggest that young time to return to the breeding grounds.
males are smaller than adult males or Apparently, at some point during its
more subordinate, so they should go stay, it fixes this exact location in its
farther south for one of those reasons memory, such that it can return to that
during their first winter. Undoubt- spot in subsequent years. Depending on
edly, some combination of factors best how philopatric the species is, a simi-
explains these patterns, too. lar pattern may occur on the breeding
grounds, where the bird has a general
Mechanisms of site fidelity target for the first year and then fixes on
a specific location it has found to be suit-
Given that so many migrants are faithful able for subsequent return trips. Thus,
to specific sites for breeding and/​or win- after its own first breeding season, a
tering, we must ask ourselves how these bird like the redstart may move between
decisions about locations are made. If a two areas of just a few hectares several
chapter 9

species shows only philopatry, it returns thousand miles apart.

to or very close to its natal area. Presum- Birds with age-related differences in
ably, these birds must have some sort of migration may use similar mechanisms

256

1stPages_B.indd 256 7/22/20 11:41 AM

 of fixing their breeding and wintering their breeding range far across the
territories, but they may not develop the temperate zone yet continue to winter in
“fixed” location until later in life. Cer- ancestral locations, often much farther
tainly this would be the second winter away than other seemingly appropri-
for a male, but it could be either the first ate habitats. Several Old World species
or second breeding season, depending have expanded their breeding ranges to
on his success the first year. Alaska or Greenland yet return to their
That there is a genetic component Old World wintering areas. Among
to these migratory patterns is shown by these, the Northern Wheatear (Oenanthe
the fact that the young of many spe- oenanthe) has breeding populations in
cies fly on their own to the wintering both Greenland and Alaska that return
grounds their first autumn. In many to their ancestral wintering grounds in
shorebird species that breed in the Africa, a journey of 5000–6000 km (fig.
Arctic, the young may fly in groups, 9.11). Of course, these extensive move-
but their parents have left before them, ments are rather recent, as just a few
so these groups must know where to thousand years ago the ice cap on the
go by themselves. Genetic control has planet limited how far north these birds
also been shown experimentally, where could breed.
young Hooded Crows (Corvus cornix) In sharp contrast to these genetically
were moved before migration and then
headed to a “wrong” location, although
Fig. 9.11. Breeding range, wintering range, and
it would have been the proper direction
migratory pathways of the Northern Wheatear
and distance from their natural breeding (Oenanthe oenanthe), which is nearly
areas.12 Final evidence for genetic control circumpolar as a breeder but maintains an
comes from species that have expanded ancestral wintering range.

Migration

257

1stPages_B.indd 257 7/22/20 11:42 AM

 programmed migrants are some species travel, when to turn, and when to stop.
that seem to have a large component In this section, we will look more
of learning involved in their selection fully at such factors as selection of
of breeding and wintering locations. routes, timing of migration, the physi-
Among these are social birds like geese, ological demands of long-range flight,
in which the young stay with their food gathering en route, and how a
parents through the winter so that they migrant orients and navigates. A variety
are taught where, and perhaps how, to of options are available to most spe-
travel. How these migrants determine cies in each of these categories, such
their movements and to what extent they that no single description of how birds
have genetic controls constitute other migrate is completely satisfactory. Given
questions about migration for which we that migratory behavior can vary from
lack information. seasonal movement across a woodland
to movement across a hemisphere, the
The Mechanics of Migration occurrence of multiple explanations for
these patterns is not surprising.
In addition to the ecological require-
ments of a species or population estab- Route selection
lishing both wintering and breeding
areas, this species or population must Evolution of a migratory route from one
evolve the means for getting from one location to another involves a variety
to the other. While the generally great of factors. Geographic or topographic
mobility of birds is such that this would barriers such as mountains or oceans
not seem to be a tremendous feat, many may be important in influencing the
of the migratory behaviors we have route taken, although these barriers are
looked at require much more than a full rather species specific. It has already
stomach and a few flaps of the wings. been mentioned that some small war-
Perhaps the seasonal migration pattern blers, along with certain shorebirds, may
of the Blackpoll Warbler (Setophaga stri- fly across the Atlantic en route from
ata) best shows the variety of adaptations North America to South America. Many
needed for successful completion of small migrants fly across the Gulf of
travel between breeding grounds in the Mexico, including the tiny Ruby-throated
Far North and South American winter- Hummingbird (Archilochus colubris). In
ing grounds (fig. 9.1a). This species uses contrast, many other species will not
a trans-Atlantic route in the fall, some- cross such water barriers. While many
times flying nonstop from New England of these are diurnally flying hawks and
to South America, but an overland route vultures, others include certain swallows
in the spring. Factors that determine and other songbirds. In some cases, this
this selection of route include weather trip around the Gulf adds many days to
patterns and prevailing winds, and a the migratory journey, even though it
variety of physiological adjustments seems as if the species could make the
chapter 9

are needed to accomplish the approxi- trans-Gulf trip. For example, we might
mately 100-hour flight required.13 The wonder why a migratory Turkey Vulture
bird must also know which direction to (Cathartes aura) that weighs several

258

1stPages_B.indd 258 7/22/20 11:42 AM

 pounds cannot match the Gulf cross- that the trade winds turn northward in
ing accomplished by the Ruby-throated the Gulf of Mexico, which assists spring
Hummingbird, which weighs only 3–4 g. migration for birds coming from the
Mountains may also be barriers, West Indies or Central America. It has
although many species can get through been suggested that the direction of the
either by flying high (migrating geese prevailing winds in this region makes
have been recorded as high as 9000 m spring migration relatively easy.16
in the Himalayas)14 or by flying through Route selection may also reflect
mountain passes. In southern Europe, history, much in the manner that history
some of these mountain passes are affects the retention of particular breed-
famous for their impressive concentra- ing or wintering grounds (see above). A
tions of migrants. Such concentrations wheatear that colonized Greenland from
apparently do not occur in the New Great Britain might follow a migratory
World because New World mountain pathway that included Great Britain,
ranges run north and south, the direc- even if a somewhat shorter route from
tion of migration. Greenland to Africa existed.
Route selection may depend on such Although examples of historical
climatic features as prevailing winds or effects on migratory routes or winter-
the use of frontal movements, factors ing areas suggest that characteristics of
that also may affect the timing of migra- migration are rather conservative traits,
tion. The migration of the Blackpoll birds actually show great flexibility in
Warbler mentioned earlier is possible their ability to adapt to changing condi-
in the fall only because of the regular tions. If we look back just 20,000 years,
occurrence of strong weather fronts that much of North America and Eurasia was
provide tailwinds for migrating birds covered with ice. Breeding and winter-
until they are well out in the Atlantic, ing areas were very different from where
soon after which these birds can use the they are today, as were migration routes.
highly predictable, northeasterly tropical Since that time, bird populations have
trade winds. Under proper conditions, changed their ranges and migration
a blackpoll is more or less blown from patterns to what we see today. Given the
New England to South America. Black- complexity of many migratory patterns,
polls will wait in New England until the this suggests rather great flexibility in
proper conditions occur and then head the evolution of migratory behavior.
out to sea. Birds that fly over the Gulf
of Mexico must also wait for the proper Timing of migration
conditions, even though this is not as
long a hop as the Atlantic migration.15 In The timing of the migration of a species
the spring, northward movement from is controlled by both ultimate and prox-
South America involves confronting the imate factors. Ultimate factors are those
regular trade winds, which pretty much evolutionary factors that are responsible
force individuals into shorter jumps for determining the basic patterns of
Migration

from island to island until they reach movement. These act over evolutionary
North America, at which time they move time to determine the average dates that
across the interior. It turns out, though, migrants arrive on and depart from the

259

1stPages_B.indd 259 7/22/20 11:42 AM

 breeding or wintering grounds. Proxi- to be closer to the breeding locations to
mate factors are environmental cues to ensure an early arrival.
which a species responds that determine Many species that breed in the
the specific date in a given year that a temperate zone migrate south long
migrant will move, including photope- before resources become limiting on the
riod, ambient temperature, wind direc- breeding grounds. This may be because
tion, flying conditions, ice or snow cover, they find it advantageous to arrive early
food availability, and other ecological to establish themselves on a territory
factors.17 within their wintering grounds, in much
Resource and breeding factors. An ulti- the same manner as the breeding birds
mate factor that determines the timing discussed above. Species that winter
of migration is variation in the overall in flocks would not have this pressure,
suitability of the breeding or wintering although no one has looked for patterns
grounds for the species. This may reflect in the timing of migration of territorial
the availability of each species’ food sup- versus flocking winter residents.
ply. For example, because of the effects For some species, the ultimate
of frost, we might generally expect determination of migration time may be
insectivores to migrate south before related to long reproductive periods or
fruit and seed eaters, nectarivores before very short breeding seasons. Arctic geese
carnivores, and so forth. This would have long enough breeding periods that
establish dates after which survival on they must go north before climatic con-
the breeding grounds would be risky in ditions are favorable so that the young
the autumn and before which migration can be old enough to fly by the time win-
would have low chances of success in ter snows arrive. Many goose species can
the spring. store enough fat and other nutrients that
The availability of enough food to they can lay their eggs and survive with
survive undoubtedly serves to put an little feeding during the first weeks after
ultimate limit to migration dates; within they arrive on the breeding grounds.
these constraints such factors as territory Tundra-breeding sandpipers do not have
and mate acquisition become import- this ability to store nutrients because of
ant in determining migration times. their small size, so they must be on the
Although many migrants arrive in the breeding grounds as soon as conditions
spring when food supplies appear to be allow to ensure successful reproduction
at comfortable levels, individuals of some before snowfall.
species, particularly males, appear to Climatic factors. Climatic factors that
arrive on the breeding ground as early as affect the ease of movement or the
possible. It appears that these individuals suitability of habitats may serve as both
may be willing to risk moving northward ultimate and proximate factors deter-
early because of the possible rewards of mining the timing of migration. To the
territory acquisition and reproductive extent that climatic factors determine
success. It has already been mentioned food supply, we have already discussed
chapter 9

how the sexes of some species winter in some of the effects of climate. We would
different areas, apparently because it is expect climatic limitations generally to
reproductively advantageous for males be most important in movement north-

260

1stPages_B.indd 260 7/22/20 11:42 AM

 ward, as such factors as late snowfall, winds may result in massive mortality
ice cover, or late leafing of trees may when the fallouts occur over water.
serve as strong selective agents against To avoid such mortality and min-
individuals moving northward too soon. imize the effort of travel, migratory
These limiting factors rarely operate birds seem to be able to recognize and
on wintering areas, although severe use various weather patterns. Since
droughts or other climatic extremes most movement is to either the north
could affect the suitability of wintering or south, migrants particularly respond
areas. In the New World tropics, a major to conditions producing tailwinds at
dry season normally ends at about the the proper time of year. These condi-
same time as winter residents prepare tions occur through the interactions of
to migrate north. On those occasions atmospheric pressure systems. In the
when the dry season extends longer than Northern Hemisphere, high-pressure
normal, spring migrants may be delayed systems have winds that blow clock-
in starting migration. wise, while low-pressure systems have
Climatic factors that affect the tim- counterclockwise winds. In the North
ing of migration in a proximate sense by Temperate Zone, these pressure sys-
influencing daily movements are most tems tend to move from west to east,
often associated with either prevailing with high-pressure systems more often
winds or winds associated with the moving from northwest to southeast and
movement of frontal systems. Most lows moving from southwest to north-
species cannot energetically afford to fly east. When pressure cells of different
into a headwind, and all find it easier to types are side by side, the winds between
fly with a tailwind. Thus, the movement the cells move in the same direction.
of weather systems can either halt or When a high-pressure cell is followed
encourage migration. In the latter case, by a low (fig. 9.12), it causes an area of
we often see what bird-watchers call winds from the south; this would be
“waves” of migrants. Researchers have of obvious benefit to spring migrants
examined patterns of migration over in the temperate zone. Since these
the Gulf of Mexico because most North lows often contain warmer air, spring
American tropical migrants use this “waves” of migrants often precede warm
route despite its length of open water periods. The reverse situation favors
(1000 km).18 It has been estimated that fall migrants. In this case, a high must
the normal flight time for a bird from follow a low, producing a region of
the southern Gulf Coast to the Yucatán southerly winds that migrants can use.
Peninsula is 24 hours, but light winds Because highs are often associated with
from the north can reduce this to 20 cold air, particularly at this time of year,
hours and strong winds to as little as 12 autumn waves of migrants often occur
hours. In contrast, winds from the south with or just before cold weather. The
produce flight times of up to 30 hours, strength of the pressure cells deter-
and under these conditions we some- mines the strength of these winds and
Migration

times see “fallouts,” where large num- the extent to which they might assist
bers of exhausted birds land on barrier migrants. Because in spring and fall in
beaches of Yucatán. On occasion, these the temperate zone there are usually

261

1stPages_B.indd 261 7/22/20 11:42 AM

 Fig. 9.12. An
example of how the
distribution of fronts
and pressure cells
can provide favorable
winds for a migrating
bird.

many pressure cells moving about, fly nonstop from New England to South
favorable flying conditions occur with America in the autumn using favorable
enough regularity that birds can wait for winds; the trade winds do not help in
their occurrence. the spring. Rather, blackpolls fly across
Tropical areas are characterized by the Gulf of Mexico and follow fronts
the more regular trade winds that blow across the eastern portions of North
from northeast to southwest in the America to their vast breeding grounds
northern tropics and from southeast (fig. 9.1a). Many migrants winter in the
to northwest south of the equator. This Greater Antilles. We assume they use
makes these winds predictably favor- a route similar to that of the blackpoll
able for migrants moving to the tropics, in the fall, following a storm out over
but their direction does not provide the Atlantic and then catching the trade
chapter 9

much help on journeys to the breeding winds and curving back to their win-
grounds. We have already mentioned tering area. In the spring, a bird from
how species like the Blackpoll Warbler Puerto Rico or Hispaniola will jump on

262

1stPages_B.indd 262 7/22/20 11:43 AM

 these trade winds and fly west, following at a time that increases their survival
these trade winds as they curve north and reproductive rates compared to indi-
above the Gulf of Mexico and provide a viduals of the same species that move at
strong tailwind for many migrants head- different times will leave more offspring,
ing to the southeastern United States.19 and thus the genes that determine
It is apparent that the existence of particular migration dates will become a
favorable winds will affect a bird’s deci- greater proportion of that species’ gene
sion about whether to leave on a partic- pool. The proximal cue that birds use
ular day or night. Aspects of this short- most often to make the decision about
term decision-making process have been migration is photoperiod. We have
examined most for night-flying birds, already mentioned how birds can moni-
because these have the greatest difficulty tor daylight periods and coordinate their
in navigating should weather conditions own internal rhythms to these changes.
change during the flight, and they have Photoperiod changes in a highly regular
a harder time aborting a night journey pattern throughout the year in all parts
because of the darkness. In general, of the world, even though the changes
though, both diurnal and nocturnal are not as pronounced in the tropics as
fliers face a similar decision-making pro- in the temperate zone. As an individual
cess that undoubtedly depends on the bird monitors the changing photoperiod,
physiological condition of the bird, the it reaches a point (probably genetically
flying conditions (especially tailwinds, determined and hormonally mediated)
storms, or rain), and the availability of where it becomes restless in preparation
appropriate cues to navigate properly for migration. The term used to describe
so that the bird does not become lost.20 this premigratory restlessness is the
Nocturnal migrants are believed to German word Zugunruhe. When this
undergo a period termed einschlaufpause state of restlessness is strong enough
early in the evening, during which they and the bird is exposed to the appropri-
sit and process all the relevant infor- ate set of short-term cues, it initiates
mation and make the decision about flight. Much has been learned about the
whether to initiate flight. Day-flying properties of Zugunruhe through experi-
migrants undoubtedly go through a sim- ments where birds have been exposed to
ilar process, but the decision is not quite altered photoperiods, sometimes pro-
as severe because it is easier for them to ducing this premigratory restlessness
navigate and simply stop should condi- at normally inappropriate times of the
tions change (unless they are over water, year.21
of course). The relative importance of ultimate
Photoperiod cues. While the einschlauf- timing cues such as photoperiod and
pause is part of the day-to-day deci- proximate cues such as climatic condi-
sion-making process, what mechanism tions will obviously vary among species
tells a bird that it is the appropriate time depending on their access to different
of year to migrate? This is obviously an cues. A bird wintering in the South
Migration

evolved trait that considers all the factors American tropics has no cues about the
we have discussed above. Those individ- conditions in its temperate breeding
uals that move southward or northward area; it times its migration following

263

1stPages_B.indd 263 7/22/20 11:43 AM

 photoperiodic cues such that it arrives The Blackpoll Warbler usually weighs
on the breeding grounds at about the about 11 g but reaches as much as 20 g
same time each year, a time that on before embarking on its flight from
average is reproductively advantageous. New England to South America. This
Variation around this arrival time will be is enough energy for 105 to 115 hours
caused by the amount of aid or difficulty of continuous flying. The Sanderling
provided by climatic patterns during the (Calidris alba), a sandpiper that makes a
migration. Shorter-distance migrants similar flight, may increase its weight to
can observe some cues about the con- 110 g instead of the usual 50 g, enough
ditions on their breeding grounds. energy from fat for a 3000 km flight if
While photoperiod is still important in aided by favorable winds.
triggering migration, these species may In addition to having energy prob-
migrate earlier in years when climatic lems, flying birds require much water,
cues suggest an early spring on their particularly when flying at high eleva-
breeding grounds. tions where the relative humidity is low.
Behavioral ecology en route. Once a bird Water balance can be a problem, but
has embarked on its migratory journey, this is usually rather easily solved by the
it must still decide a variety of things metabolic water that is manufactured in
in addition to direction. The height at converting fat into energy.
which it should fly is one of these. Most A particular flight may end because
small passerines fly at about 2000 m the energy reserves of a migrant are
altitude, while swans and geese have diminished, or because there is a change
been known to fly as high as 9000 m, in wind direction or some other factor.
where the temperature is −28°C. This Before continuing, the migrant needs to
decision may be adjusted according restore its fat reserves. This necessitates
to the height at which the maximum high feeding rates during its migratory
tailwind is achieved. Some diurnal stopover periods in what may be atyp-
migrants use thermals or other air ical habitat. Some work has suggested
disturbances to aid their movement.22 that migrants show patterns of habitat
As we mentioned in chapter 3, migrat- selection while moving, although the
ing storks can fly at almost no energetic short-term nature of most visits results
cost with the proper air currents. Hawks in great variability in habitat use. A few
and other raptors also use thermals to migrants are known to set up territories
assist in migration, while oceanic birds and defend feeding grounds while en
undoubtedly use dynamic soaring. route; among these are hummingbirds,
Whether soaring or flapping, which apparently get enough rewards
migration takes energy. Most birds store from the flowers they defend to justify
this energy as fat before they take off the costs of defense over short periods.
for each trip, as fat provides the most Most migrants are known for their
calories per mass of any food. Long-dis- flexible food habits, particularly while
tance migrants undergo what is known traveling. Virtually any food with energy
chapter 9

as hyperphagia, a form of feeding is worth harvesting to help accumulate

frenzy that may nearly double their fat reserves. By foraging all day long,
body weight before they leave on flights. migrants can develop enough fat to

264

1stPages_B.indd 264 7/22/20 11:43 AM

 travel again that night or the next day, redundancy in its navigational systems,
should conditions warrant. The fairly as making a mistake in a behavior as
predictable patterns of movement of costly as migration could have severe
large numbers of birds have led to some negative effects on an individual. We
coevolutionary patterns with flowering must keep this flexibility in mind as
or fruiting plants, where the plants we look at some of the mechanisms
apparently time their flowering or migrants use to navigate.
fruiting to coincide with the movement Studies in avian navigation are
of migrants. For example, the spring distinctive because of their experimen-
blooming of the Red Buckeye (Aesculus tal nature. While we can learn about
pavia) of the southeastern United States migratory routes and the locations of
has historically coincided with the north- breeding or wintering grounds through
ern migration of its chief pollinator, observation, aided by marked individu-
the Ruby-throated Hummingbird. This als or such sophisticated observational
gives an individual plant a chance to pol- techniques as radar, trying to under-
linate another plant perhaps hundreds stand the directional decision-making
of miles away. As biologists learn more process of a migratory bird requires
about tropical plants, they are discover- much more ingenuity. Most navigational
ing more and more species that seem to studies of migrants involve capturing
time either fruiting or flowering to use birds and exposing them to experimen-
this horde of ravenous migrants for pol- tal situations (changes in star patterns,
lination or fruit dispersal. Unfortunately, photoperiod, and such). Much has also
there is some evidence that global warm- been learned about navigation by using
ing may be disrupting the synchrony of homing pigeons, which are often much
these patterns. easier to manipulate than wild birds. As
we will see, other studies have gone as
Navigation and orientation far as strapping electromagnets on birds
to see whether orientational abilities can
The process by which a bird determines be affected.
which direction to fly and when to stop Before looking at the mechanisms
and remain in a particular location of navigation, we must recognize that
includes aspects of navigation (choosing species vary in their overall naviga-
a path), orientation (figuring out where tional abilities. Although many species
it is), or both. Questions about these can find exact locations on both their
movements have puzzled scientists for wintering and breeding grounds, they
many years, and although some brilliant do not have complete navigational and
work has been done, complete answers orientational abilities. Rather, they can
have not yet been achieved. This lack of move in the proper direction for the
success may arise in part because differ- correct distance; if displaced from their
ent species use different systems of navi- natural location, they cannot find their
gation, and because it appears that most way back to it. Numerous studies have
Migration

species have several alternate systems to shown this lack of flexibility in move-
use as backups should one fail. It is not ment, including translocations of large
surprising that a bird should have some numbers of Hooded Crows, European

265

1stPages_B.indd 265 7/22/20 11:43 AM

 Fig. 9.13. Normal distribution of recoveries of
European Starlings (Sturnus vulgaris; red
dots) banded at The Hague, Netherlands (blue
dots), compared to recovery locations of adult
starlings (green) and juvenile starlings (orange)
that were displaced from The Hague to
Switzerland. Note that many adults returned
to their proper location, but juveniles tended
to move the distance and direction they would
have moved had they not been translocated
(Perdeck 1958).

of homing have been recorded, including

a Manx Shearwater (Puffinus puffinus)
that returned 5300 km in just 12.5 days.24
A problem that sometimes confuses
studies on navigational abilities is the
distinction between selecting a route
and maintaining a particular direction.
Once a route has been selected, rel-
atively few cues are needed to help a
bird maintain that direction. The initial
selection process is most important, but
studies often have trouble separating
the cues used for selection versus those
Starlings (Sturnus vulgaris; fig. 9.13), and used to maintain direction.
storks.23 These studies show that these Early studies on the mechanisms
species, at least when young, have only of navigation tried to identify a single
the ability to navigate (use a compass cue that birds used. Recent studies
to find the appropriate direction and have led us to realize that birds use
distance), but they are apparently unable multiple cues. The existence of multi-
to orient themselves and realize they are ple cues makes studies on navigation
not in the “proper” location. True bico- mechanisms that much more complex,
ordinate navigation means that a bird though, because the scientist must be
can find its way back to the appropriate sure that the experimental birds are not
location when displaced, suggesting that using cues for navigation or orientation
it knows where it is in addition to the other than those being manipulated.
normal direction and distance of travel. A wide variety of navigational cues
Unlike young birds, adult starlings seem have been suggested as being important
to show some ability to both navigate and to birds. Among these, cues from the
orient themselves. Bicoordinate navi- sun, stars, and the earth’s geomagnetic
chapter 9

gation is well developed only in certain field may be ranked as of major impor-
seabirds, swallows, and pigeons. Among tance, particularly in the initial selection
these, some rather impressive examples of a migratory route. Secondary factors

266

1stPages_B.indd 266 7/22/20 11:43 AM

 that aid a bird in maintaining its route itself at 90° off the correct direction.
but that seem less important in route The location of the setting sun
selection include topographic features, seems to be important to many noctur-
wind movements, auditory signals, and nal migrants. On nights when the sun
perhaps even odors from the ground. is hidden by clouds, migration may not
Solar cues. The position of the sun occur or shows greater variation in direc-
seems to be one of the prime naviga- tion. As long as a bird can see the setting
tional cues for both nocturnal and diur- sun or even the lighted western sky for
nal fliers. Using the sun as a compass a brief period, however, it appears to be
requires compensating for its move- able to select the proper direction.
ment across the sky, which birds seem Although there is conclusive evi-
to be able to do by synchronizing their dence that birds can use the sun as a
internal biological clock with the sun’s compass, it is not clear that birds can
movements. Some of the best experi- use the sun to determine their exact
ments on the use of the sun as a com- geographical location. Experiments with
pass are those where birds are exposed pigeons suggest that they can detect the
to different photoperiods such that the polarization of light, which they could
time their body thinks it is differs from use for such orientation, or perhaps
the actual sun time (so-called clock-shift birds can correlate the position of the
experiments; fig. 9.14).25 A bird clock- rising and setting sun with the proper
shifted six hours from sun time orients biological clock to measure latitude.

Fig. 9.14. Variation in observed departure

bearings of pigeons whose clocks were
advanced by six hours and then were released
30 to 80 km north, east, south, and west of
their home lofts. Arrows denote mean direction
(Keeton 1969, 1974).

Migration

267

1stPages_B.indd 267 7/22/20 11:44 AM

 Whereas much work needs to be done
on all the information the sun provides,
it is clear that solar cues are important to
nearly all migrants.
Stellar cues. Stellar cues would obviously
be important only to nocturnal migrants.
To determine the importance of stellar
cues in orientation, caged birds exhib-
iting Zugunruhe have been exposed to
altered night skies in planetariums.26
By using cages with perches that record
where the bird sits, researchers can see
the direction these birds want to travel
given certain patterns of stars. Exper-
imenters have been able to shift the
direction of orientation of birds by up to
180° by shifting the apparent night sky Fig. 9.15. Experiments with stellar navigation
by an equivalent amount (fig. 9.15). in the Indigo Bunting (Passerina cyanea). The
Although the above studies show diagrams measure the direction of activity of
how birds use the stars as a compass, it caged birds that were exposed to the natural
is more difficult to see whether they can sky in the spring (top left), to a planetarium
also use them for bicoordinate naviga- showing the natural sky (top right), to a
tion. To do this would require proper planetarium with the sky rotated 180° (bottom
left), and to a darkened planetarium (bottom
synchronization with a biological clock,
right) (Emlen 1967).
especially since star patterns change so
much both latitudinally and through
the year, as well as through the night.
Experiments suggest that long-distance effects on navigation. The results have
migrants may be able to use the stars for shown that most birds can use a variety
both direction and measuring latitude, of stellar cues to select or maintain the
while shorter-distance migrants seem proper direction.
to use stars only as a compass. Much Geomagnetic cues. Geomagnetism is
variation, among both species and indi- perhaps the most controversial and
viduals, seems to occur in which partic- least understood of the major possible
ular stars are important for navigation. navigational cues. A variety of evidence
Indigo Buntings (Passerina cyanea) seem suggests that birds can detect the earth’s
to use the northern sky, within 35° of the magnetic field and may be able to use
North Star, for most of their navigation, it for navigation. The best studies are
while those species that migrate to the with pigeons, where the addition of
Southern Hemisphere must use a larger small magnets or Helmholtz coils (small
portion of the sky. Researchers have electromagnetic devices) to the pigeon
chapter 9

tried a variety of planetarium experi- causes disorientation under controlled

ments where part of the sky or certain conditions (fig. 9.16).27 A possible mech-
stars were darkened to see possible anism for such electromagnetic detec-

268

1stPages_B.indd 268 7/22/20 11:44 AM

 tion was identified with the discovery cues, the location of sunset, and perhaps
of concentrations of the ferromagnetic geomagnetism. Numerous studies have
mineral magnetite (Fe3O4) at several shown that on cloudy nights there is
locations in the pigeon’s head. Treat- more scatter in the directions chosen by
ments that chemically rearranged the migrants. Yet even under these condi-
magnetic elements in the pigeon’s head tions, most migrants appear to travel in
resulted in disoriented flight. the proper direction, and if stellar cues
Experiments attempting to measure are obliterated by cloud cover during
geomagnetic navigation in other species the night, the proper direction is main-
have been less successful. Several Euro- tained. Obviously, other cues are used,
pean species have been placed in a steel especially to maintain the proper orien-
chamber (which reduced the intensity of tation. Wind direction seems to be an
the earth’s magnetic field) and seemed important backup cue. Once a migrant
to lose their ability to orient correctly. has selected the proper direction using
When large Helmholtz coils were placed the above cues, all it may need to do to
around test cages, predictable changes stay properly oriented is to maintain a
in orientation were recorded. Unfortu- direction relative to the wind. Disorien-
nately, some of these studies have not tation among migrants tends to occur
been reproducible, so the importance of only when clouds are associated with
geomagnetic cues in most species is still foggy, windless conditions. Although
poorly understood. evidence has suggested that topographic
Other cues. Most migrants probably features are important only in deter-
select their direction of travel using mining final destinations for nocturnal
some combination of solar and stellar migrants, they could aid a migrant
Fig. 9.16. Pigeon wearing
Helmholtz coils as part
of experiments on the
role of magnetism in
bird navigation and
orientation (Wiltschko
1968, 1972).
Migration

269

1stPages_B.indd 269 7/22/20 11:44 AM

 when other cues fail. Even on the systems in recent years, in many ways
darkest night, enough landmarks may we have only scratched the surface.
be apparent to help with orientation.
A bird flying at about 600 m elevation The Evolution of Migration
can see about 100 km around itself on
a clear day. While this would be greatly With the tremendous variation in the
reduced on a cloudy night, topographic characteristics of migrant birds, it is
cues might still be of use. Sounds from not easy to answer the question, why do
the ground (a waterfall, the ocean) could birds migrate? Quite obviously, migra-
also help a bird maintain its course. tion must be evolutionarily adaptive
Finally, it has been suggested that to occur in a species, but with all the
odors may be of assistance. It should be comings and goings within each habi-
noted that many of these backup cues tat, it is difficult to come up with a nice
require experience to be useful. Since general way to explain migration. More
many migrants make at least one trip often, we must ask why some, but not
alone without such prior experience, all, species in a habitat migrate.28
they serve only to assist the experienced Although we cannot expect concrete
migrant when other cues fail. It should answers to the above questions, we can
also be noted that many migrating birds get some idea of the various selective
make mistakes, despite these backup factors that different species seem to be
cues. Such mistakes are most appar- balancing in evolving either migratory
ent in coastal situations, where many or sedentary behavior. The resulting
migrants can be seen flying back to land trade-offs must blend in a way that is
after overshooting the coast. adaptive for the individual; too many
Most migrants seem to be able to costs without any benefits will not allow
use several of these cues for navigation, an individual to survive and will lead to
although the importance of each varies the loss of these traits within a species.
among species. Savannah Sparrows In many cases, only relative differences
(Passerculus sandwichensis) navigate in the strength of the factors that affect
primarily by the stars, but they are more migration will determine which species
accurate when they have a chance to view can stay in a location and which must
the sunset. Those European species that migrate (or at least find it evolutionarily
apparently use geomagnetic forces seem advantageous to migrate). To explain
to calibrate them with stellar patterns. these trade-offs properly, we must
Further research will probably find an consider both breeding and wintering
infinite number of variations in the use areas, comparing the relative trade-offs
of these cues. Given the importance of found in species that have bred together
accurate navigation, it is not surprising but face an inclement period (temperate
that multiple cues exist, for they allow a breeders), or in species that have sur-
bird to calibrate with accuracy and adapt vived a nonbreeding period and face an
to changing weather conditions so that it approaching reproductive decision (on
chapter 9

survives the journey. Although we have the wintering grounds).

learned much about avian navigation The three major factors that involve
trade-offs in our model are reproductive

270

1stPages_B.indd 270 7/22/20 11:44 AM

 success, mortality rate, and site domi- once they reach adulthood. Thus, we see
nance. Reproductive success is obviously relative survivorship benefits to migra-
important to the evolution of migratory tion relative to temperate residents, but
behavior in a species; individuals with survivorship costs of migration relative
distinctive migratory traits may produce to tropical residents.
the most young and leave the greatest The final factor, site dominance,
proportion of their genes in the popu- includes a variety of subfactors related
lation, thus influencing the migratory to acquisition of food or nest sites.
traits of that population. Reproductive The trade-offs involved here are less
success is a function of clutch size, clear, but several generalizations seem
number of broods, nest predation, reasonable. At the temperate breeding
and factors related to food availability grounds, it appears that permanent
(both climatic factors and the degree of residents generally have dominance over
crowding due to the number of compet- migrants, especially for nest cavities.
ing species). In general, temperate areas Such cavities are limited in number,
provide great amounts of food during and permanent residents can occupy
the summer, so that larger clutches can them before migrants arrive, thereby
be laid, and perhaps more broods can be achieving site dominance. In general,
raised (see chapter 12 for a discussion of 50%–70% of cavity nesters in the tem-
clutch size variation). Temperate zones perate zone are residents, while only 5%
also seem to have lower rates of nest of open nesters are residents. Cavities
predation than tropical areas. A bird that apparently provide protection from
breeds in the temperate zone can pro- predation and thereby increase nesting
duce more young on average each year success and permit a larger clutch size;
than a similar bird could if it bred on the the first birds to get these cavities seem
tropical wintering area. Among temper- to be able to keep them. Finally, there
ate breeders, however, permanent resi- is some evidence that dominance in
dents raise larger and frequently more acquiring good roosting sites may be a
broods than species that migrate from factor influencing migration.
the tropics. This gives a crude hierarchy Site dominance on the wintering
of potential reproductive success of tem- grounds must also be considered.
perate permanent residents > migrants Although less is known about the
> tropical permanent residents. nesting habits of tropical birds, cavity
Mortality rates vary markedly among nesters there also have lower predation
temperate residents, migrants, and rates, but cavities are limited in number.
tropical residents. Temperate residents Species without enough dominance to
must face the hardships of winter, and acquire or maintain a cavity would be
average survival rates for these birds forced to nest in more predator-suscep-
are relatively low. Migrants experience tible open nests, with lower chances of
relatively large juvenile mortality during success.
the first migration, but adult migrants Food acquisition traits may also
Migration

have greater survivorship than temper- affect general site dominance. Species
ate residents. Tropical residents appear that are behaviorally subordinate may be
to have the lowest mortality rates of all, “forced” from an area during resource

271

1stPages_B.indd 271 7/22/20 11:44 AM

 shortages. In the temperate zone, these relative trade-offs are the reverse. Per-
species perhaps could survive the winter manent tropical residents have higher
in the absence of more dominant com- survivorship rates than migrants, but
petitors, but the presence of these domi- they also have very small clutches and
nants keeps them away from the limited thus lower reproductive rates. Those
food supply and forces them to leave migrant species that only winter in the
the area. Similar differences in domi- tropics face higher adult mortality rates
nance among species in tropical areas than species that do not migrate, but
could mean that some species find food this is compensated for by the larger
gathering harder during the breeding clutch sizes they can produce in the
season, when the additional stresses of temperate breeding grounds. Evidence
feeding young make food more limiting. that permanent residents in the tropics
These subordinate species might be dominate migrants is less convincing;
more prone to migrate to other nesting early studies of interactions between
grounds. these groups suggested that winter
How might the variations in these residents were more or less forced to
characteristics fit together to better feed on “leftover” resources,30 but recent
explain which species migrate? In the work has shown that many winter
temperate zone, permanent residents residents seem to have stable positions
seem to be those species whose behav- as part of tropical bird communities.
ioral dominance allows them to acquire Whether these tropical migrants are
enough food to survive the winter and “forced” northward is really not criti-
gives them access to nesting cavities cal, as long as we can see differences
or the best nest sites for breeding (fig. between the balances of survivorship
9.17).29 The latter factor allows greater and reproduction in the two groups.
reproductive success, but this produc- Many tropical-wintering migrants seem
tion actually only balances relatively to have more flexible foraging behavior
high winter mortality. Migrants from than permanent residents; while this
the temperate zone are unable to find more generalized behavior may make
enough food in winter to survive, either them less successful competitively when
because it is totally unavailable or resources are limited (breeding) or may
because interactions with more domi- simply preadapt them for long journeys
nant species make it inaccessible. These with variable diets, it suggests some for-
migrants also have less chance to gain aging differences that may affect migra-
access to cavities, so they more often tion strategies.
nest in the open, have relatively smaller This rather simple model allows us
clutch sizes, and frequently nest only to make some predictions about differ-
once. This lower relative reproductive ences between migrants and residents
output is balanced by the higher survi- that we can measure, and it helps
vorship these species achieve by spend- explain a variety of observed differences
ing the winter in the tropics (although between these groups of birds. Although
chapter 9

juvenile mortality during the first trip we have talked in terms of temperate-
may be high). tropical comparisons, we can modify
On the wintering grounds, the this model to within-habitat trade-offs

272

1stPages_B.indd 272 7/22/20 11:44 AM

 Northern Forests:
Many migrants, few
residents. Harsh
winter conditions
limit species survival.
Migrants attain
greater reproduction
than possible on
wintering grounds
at cost of migration
losses. Residents
balance high winter
mortality with high
breeding success,
in part through site
dominance.

Greater Antilles:
Many migrants, few
residents. Migrants
get advantage of
species-poor areas
in winter but avoid
Mexico and Central constraints of
America: Many tropical islands when
migrants and many breeding.
residents. Mild
climate results in
high winter survival
while short distance
to temperate zone
makes migration
for breeding a good
strategy.

Amazonia: Many
residents, few migrants.
Residents show high
survivorship but low
reproductive rates.
Distance to temperate
Migration

Fig. 9.17. A summary of the trade-offs zone too great for

associated with migratory strategies in different migration to be adaptive.
parts of the New World (Fretwell 1980).

273

1stPages_B.indd 273 7/22/20 11:45 AM

 that might occur in either temperate or is the effect of being a migrant?), food
tropical habitats. For example, in trying habits of migrants versus residents (are
to explain why some hummingbirds migrants really subordinate, or more
migrate from the tropics while others generalized, or adapted to edge or sec-
stay put, we would want to look at the ond-growth habitats?), and other aspects
characteristics of each species in terms of behavior (are flocking species more
of survivorship, reproduction, and, likely to migrate?). Although we have
perhaps most importantly, dominance a better idea of which sorts of species
interactions at flowers within the win- migrate, there is a confusing array of
tering zone. Subordinate hummingbird strategies within these general patterns.
species may have more to gain overall This confusion is compounded by the
by going elsewhere to breed, even if historical effects that may influence
elsewhere is only up a mountain slope migrant strategies. Within the Greater
within the tropics. Antilles of the West Indies, there are
We have already shown that some large numbers of wintering warblers
species exhibit sex- or age-related and (as shown in chapter 5) relatively
differences in migration; the site domi- simple resident insectivorous bird
nance factor of our model explains this communities. These migrants gain the
rather nicely. Site dominance might also advantages of survival through the West
suggest that species should go only as Indian winter plus the greater reproduc-
far south as they absolutely need to, so tive success of the temperate summer.
that they can get back to the breeding At about the same time that this large
grounds as early as possible (or back to group of winter residents leaves the
the wintering grounds for site domi- Greater Antilles, two or three species
nance there). This factor, combined with enter these islands from their wintering
intraspecific competition, may lead to grounds in South America. These spe-
what is known as leapfrog migration, cies breed and then migrate back to the
where the southernmost breeders of a south, although these same species do
species winter the farthest north and not migrate on the smaller Lesser Antil-
the northernmost breeders the farthest les, where few winter residents exist. In
south. The northernmost populations this case, it appears that the West Indian
may be able to stay put or move only summer residents are taking advan-
short distances, possibly giving them tage of resources “left” after the exit of
dominance over migrants from farther the temperate breeders, a strategy that
away, which may also arrive later. These likely evolved after that of the temperate
migrants from the north may then move migrant species.
southward enough to avoid competition Quite obviously, there is much to
with the southern breeders, which forces do to develop a more comprehensive
more northerly breeders even farther theory of the evolution of migration. It is
south, and so forth. inevitable, though, that models explain-
Other factors that require further ing this behavior will be either extremely
chapter 9

examination include the dominance general, so they can cover the vast vari-
factors that affect hole versus open ety of migrant strategies, or specific only
nesting (which is the cause and which to particular migrant situations. With

274

1stPages_B.indd 274 7/22/20 11:45 AM

 increasing knowledge of the population breeding numbers. Recent work on spe-
and behavioral characteristics of both cies with limited stopover sites during
migrants and residents, however, we migration has shown that loss of food
should be better able to explain the strat- at these sites has resulted in declining
egies behind the many wonders of bird populations of these migrant species,
migration. irrespective of how much wintering
or breeding habitat they have and how
Conservation of Migratory Birds good it is.31
Within the past 25 years we have rec-
Although the focus of this book does not ognized that migrant birds may require
include conservation and management management activities throughout their
of bird species, it must be noted that annual cycle. A symposium in 1989
the incredible flexibility of movement documented that migrant bird popu-
in migratory birds also presents con- lations were declining more than any
servation challenges with these species. other group; this led to the formation
Within the span of a year, a migrant of Partners in Flight, which has been
species has both breeding habitat described as the world’s largest conser-
requirements and wintering habitat vation effort.32
requirements, plus the migrant species Developing the ecological knowl-
has to find enough fuel in appropriate edge that would allow us to manage
habitats to be able to make the often species that move around so much
long-distance movements their migra- through their annual cycle is extremely
tion requires. This annual cycle may challenging, but we have made tremen-
involve two to four months of resi- dous advances in recent years.33 Breed-
dency on a breeding site, up to seven or ing-season studies originally focused on
eight months on a wintering site, and how loss and fragmentation of habitat
a month or even more of movement affected reproductive success of migrant
between these two disparate locations birds, including studies showing that
during both spring and fall. While we many species required minimum areas
know that loss of breeding habitat could of habitat to produce young. On smaller
result in reductions of a migrant spe- habitat patches or near the edges of
cies’ population because of insufficient larger patches, nest predation rates and
reproduction, others have noted that cowbird parasitism rates were extremely
loss of the appropriate wintering habitat high, often resulting in the near total
could also serve to limit populations, failure to produce young. Recently, these
and it is clear that having proper habitat nesting studies have been extended
during migration can be critical. John into the postfledging period, which
Terborgh (1980) noted that the concen- includes a period of several weeks when
tration of wintering birds in Mexico, fledglings are still under parental care,
Central America, and the West Indies followed by a longer period when young
was such that a hectare of wintering birds are independent and preparing
Migration

habitat supported the birds from 8 ha or for fall migration. For some species, the
so of breeding habitat. Loss of wintering independent postfledging stage involves
habitat would have extreme effects on a total shift in habitat. For example, in

275

1stPages_B.indd 275 7/22/20 11:45 AM

 the Missouri Ozarks, Ovenbirds (Seiurus recent years there has been an increase
aurocapilla) nest and the fledglings stay in our ability to follow groups of birds
in mature forest for the first three weeks with radar as well as individual birds
after fledging, but at independence, carrying devices (see below). In general,
these young birds make a total shift in though, studies during migration are
habitat, moving into clear-cuts and other difficult.
short forest habitats for the remainder To do good science regarding migra-
of the summer.34 Optimal forest man- tory bird populations, we need to be sure
agement for species such as Ovenbirds that we are studying the same individu-
includes provision of both mature als throughout the annual cycle, a phe-
nesting habitat and early-successional nomenon known as connectivity. If all
postfledging habitat within the same the Ovenbirds that breed across North
general region. America scatter widely across the win-
Studies on the winter ecology tering range, there will be low connectiv-
of migratory birds have focused on ity such that studies of breeding season
­winter habitat selection and its effects demography or winter survival will be
on survival, which is the main focus of limited value because the birds come
of the often long (up to eight-month) from such a broad region. On the other
winter season. Many migrants are very hand, if Ovenbirds from the eastern part
site faithful, which allows researchers of their breeding range travel mostly to
to ­capture birds over many years and the eastern part of their wintering range,
measure habitat selection and survival there will be higher connectivity and we
rates; some species are very nomadic may be able to understand the demo-
and make such measures nearly impos- graphic patterns of this subpopulation.
sible. Winter research has shown that With increased knowledge of patterns of
many species have sex-related patterns of connectivity, we can get a better idea of
habitat selection, sometimes including which factors might be affecting pop-
aggressive encounters. Long-term stud- ulation change in different parts of a
ies in a dry forest in southwestern Puerto species’ range and respond accordingly.
Rico found that the wintering popula- Unfortunately, measuring connec-
tions of Black-and-white Warblers and tivity is difficult. Banding thousands
American Redstarts are 90% or more of migratory birds has resulted in little
female; males may dominate in other information on movement patterns,
vegetation types such as mangroves.35 because the number of birds banded has
Studies of stopover ecology during been tiny relative to the total populations.
the two migratory periods of the year Banding has been critical to measuring
are more difficult to conduct because site fidelity and other traits of both breed-
most bird species are small and difficult ing and wintering birds, but the recap-
to track over long distances. Bird move- ture rates of banded birds away from
ments can be observed by birders; the their banding site are extremely low.
accumulation of such observations at A breakthrough a few years ago
chapter 9

the Cornell Lab of Ornithology through discovered that the levels of the isotope
eBird has resulted in some astound- deuterium in a feather reflected where
ing maps that document migration. In that feather was formed. Collecting tail

276

1stPages_B.indd 276 7/22/20 11:45 AM

 Fig. 9.18. Suggested
connectivity between breeding
range and wintering range as
determined by use of stable
isotopes from feathers removed
from American Redstarts
wintering in a single location
in southwestern Puerto Rico
(Dugger, Faaborg, Arendt, and
Hobson 2004).

1stPages_B.indd 277 7/22/20 11:45 AM

 feathers from the wintering grounds, weight device rides on a small bird’s
analyzing them for deuterium, and then back and has a clock and light sensor
comparing that level of deuterium to on it. The clock records the time of day,
the level of deuterium in rainfall across while the sensor records sunrise and
North America gave a pretty good esti- sunset. With those two measurements,
mate of where the feather was formed, you can determine your location on the
and most likely where the bird bred planet at any time of the year except
(although molt migration affected this around the equinox, when day length is
pattern in the western United States). equal.
This pattern worked well in the east- All researchers had to do was buy
ern United States because deuterium a small handful of these, put them on
and rainfall tend to follow a latitudinal study individuals that they assumed
pattern there; the relationship with would return to that location the next
rainfall and deuterium is much more year, and then wait a year until the
complex in the mountainous west. Stud- bird returned and they could catch it
ies from tail feathers provided insight to remove the geolocator. The device
into general patterns of connectivity would tell them exactly where the bird
for many species (fig. 9.18). Studies of had traveled during the past year, except
genetic patterns provided similar results, for a week or two around March 21 and
although these involved somewhat more September 21. Geolocators have been
work than just collecting a feather and of great value in providing data on
analyzing it for heavy water. Both these connectivity, migratory pathways, and
methods provided general measures of even basic observations such as winter
connectivity, but there was always some range. With geolocators, we discovered
unknown amount of variation in the that some swifts apparently do not rest
measurements. during the winter but fly all night long,
Radio-tracking devices have been shutting down half their brain while the
developed in recent years that allow the other half keeps the bird aloft.
use of satellite transmitters to record Hundreds of geolocator studies
the movement of large birds across the are currently underway, and most are
planet through the year. Such radios are providing extremely interesting insights
much too heavy to fit on most of the into migration. Some combination of
small migratory birds that are of con- geolocator and stable isotope data will
servation concern, and even if they are undoubtedly give us more information
light enough to use, their signal travels on patterns of connectivity in migratory
only a few kilometers at best. While this birds, information that will be critical to
is good for studies of local movements, understanding migrant bird population
once a bird moves a few miles, it is declines and what can be done to stop
gone. A few years ago, the light-sensitive them.
geolocator was developed.36 This light-
chapter 9

278

1stPages_B.indd 278 7/22/20 11:45 AM

 C HA PT E R 10

Anatomy and Physiology

of Reproduction

M
ost anyone who eats break- Producing an Egg
fast with any regularity is
familiar with the key to Reproduction serves two important
avian reproduction, the purposes. Obviously, it is the way an
egg, and knows that it comes in a variety organism reproduces itself so that
of sizes ranging from very small to extra some of its genes survive in subsequent
large. Unlike the other classes of verte- generations. Of perhaps equal impor-
brates, birds exhibit only egg laying (ovi- tance, though, is the fact that reproduc-
parity) as a reproductive strategy; they tion allows an organism the chance to
cannot retain young and nurture them produce, through sexual recombination,
until birth as mammals do (viviparity), offspring with varying genetic traits
and they do not retain eggs within the that may affect survival in the future.
body until they hatch, as some reptiles The occurrence of sex is costly: if males
do (ovoviviparity). Yet within this seem- were not necessary, all birds could
ing constraint, birds show remarkable produce eggs, potentially doubling the
variability. For example, while most production of young. However, the lack
eggs hatch with young that are entirely of variability resulting from a single-sex
dependent on parental care, some young system would be maladaptive; the costs
are totally self-sufficient when they hatch of a two-sex system are more than com-
and are immediately able to feed and pensated for by the production of young
care for themselves. with a variety of genetic characteristics.
Associated with this variation in Although a two-sex system is adap-
egg characteristics are specific traits of tive, it does not necessarily represent a
egg composition, parental care, growth balanced division of reproductive effort.
rates, fledging times, and so forth. In Only females produce eggs, and these
this chapter, we will discuss the general eggs require a much greater investment
mechanics of reproduction, with empha- of energy than the sperm produced by
sis on both the constraints faced by vari- the males. While males may try to com-
ous types of birds and the flexibility they pensate for this imbalance in a variety of
may have. We begin with a brief look at ways (see chapter 12), this asymmetry in
the basic anatomy and physiology of egg the initial costs of reproduction cannot
production. be ignored.

279

1stPages_B.indd 279 7/22/20 11:46 AM

 We have briefly mentioned the The ovary is situated in the center of
morphology of the avian reproductive the body cavity, anterior and ventral to
tract in earlier chapters. There we noted the kidney. During the breeding season
that it was seasonally variable in size to it may enlarge up to 50 times with the
better accommodate flight and that it development of several mature ova (sin-
was associated with the urinary tract. In gular, ovum). The ovary contains hun-
the female, the apparent selection for dreds of thousands of oocytes, but only
reduction in weight has resulted in one a very few of these develop during each
functional reproductive tract in what breeding period. The oocytes that do
originated embryologically as paired develop move from the outer layer of the
tracts. In all birds, the left side of the ovary to the center or medulla, where
reproductive tract is developed. In most they become surrounded by concentric
species, the right side is only rudimen- layers of vascularized ovarian tissue,
tary, although in some birds of prey and forming a follicle. The follicle protects
in kiwis a mature right ovary is present and nourishes the oocyte during its
and functional. development and passes to it the lipids
and proteins synthesized in the liver
The female reproductive system (vitellogenesis). These materials form
the large inner mass that we recognize
The female reproductive system consists as the yolk of an egg. At first, follicular
of an ovary and an oviduct (fig. 10.1).1 growth is slow, and it may take months

Fig. 10.1.
Reproductive
chapter 10

organs of a female
chicken (Romanoff
and Romanoff
1949).

280

1stPages_B.indd 280 7/22/20 11:46 AM

 to years for the oocyte to grow only a function. Ciliated cells in the infundibu-
few millimeters in diameter. Then, over lum, or mouth, direct the ovum into the
a period of several weeks there is rapid oviduct by an active process that works
deposition of protein in the yolk, and only at the time of ovulation. Usually
finally, a short period of extremely rapid fertilization occurs here within 15 min-
growth occurs during the 7–11 days prior utes of ovulation. The ovum then moves
to ovulation, when lipids synthesized in into the magnum, a thicker part of the
the liver are added to the yolk. During oviduct. Fertilization must occur prior
the latter period in the chicken, the fol- to the ovum’s arrival, before more layers
licle enlarges from an initial 8 mm to 37 are added to the yolk that could impede
mm in diameter and increases in weight sperm entry. The magnum retains the
from 0.08 g to 15–18 g. The oocyte ovum for two to three hours while sev-
undergoes one meiotic division during eral layers of albumen, or egg white, are
development; the second meiotic divi- added. Once this is done, the egg moves
sion is initiated at fertilization, so that to the isthmus, where the two keratin
only half of the parental complement of shell membranes are applied, a process
DNA remains. that takes one to five hours. The final
The development of the follicle construction of the egg is completed in
and the oocyte is regulated by follicle-­ the uterus or shell gland, where a watery
stimulating hormone (FSH) secreted by albumen layer is added, and the egg is
the anterior pituitary gland. When the sealed with a calcareous shell and a cuti-
follicle reaches maturity, the outer layers cle. Pigments that are added to the shell
break down, and under the influence during the 20-hour shell-forming pro-
of another anterior pituitary hormone, cess are secreted by uterine glands. The
luteinizing hormone (LH), the follicle colors are derived from bile and blood
ruptures, releasing the mature ovum (hemoglobin) pigments, and the pat-
into the body cavity. This is the process terns are a result of the movement of the
known as ovulation. The ovum does not egg in the shell gland. Near the junction
float aimlessly in the body cavity because of the vagina and shell gland is a region
the waving fimbria of the anterior end with simple columnar epithelium; here
Anatomy and Physiology of Reproduction
of the oviduct, called the infundibulum, are the sperm storage tubules that can
draw it into the mouth of the oviduct. store sperm for up to two weeks.2 The
The role of the oviduct is to com- vagina is the last region of the oviduct.
plete the construction of the egg by It lubricates the passage of the egg by
providing a watery albumen layer to mucous secretions and its muscular
buffer the yolk and a protective shell, walls move the egg to the cloaca. This
and to move the egg to the cloaca. Most region is also important for the collec-
birds lay an egg a day, and ovulation tion and storage of sperm (see below).
often occurs just after laying so that only The above process of egg formation
one egg is present in the lower part of requires significant energy expenditure
the oviduct at a time. The oviduct (also by the female. For example, a female
called the Mullerian tube) is a long, House Sparrow (Passer domesticus) lays a
winding tube that can be divided into clutch of four to five eggs, whose energy
five segments, each with a different content is 14.4 kcal. If the total time for

281

1stPages_B.indd 281 7/22/20 11:46 AM

 production of these eggs is about 7.7 fat reserve because the number of eggs
days, and her efficiency in converting produced is closely correlated with their
assimilated energy into egg material is weight on arrival.
about 77%, then the energy requirement
for egg laying would be 2.4 kcal per bird The male reproductive system
per day. This cost represents a 26.6%
elevation of her basal metabolism. In In contrast to this enormous energetic
addition, many physiological changes undertaking in the female, the male pro-
occur in the female that enable her to vides only the spermatozoa to fertilize
rapidly synthesize and deposit nutrients each egg. Although of little energetic
in the yolk. A laying bird typically has value, each spermatozoan is critical for
a blood glucose concentration that is the genetic information it contains, as
about twice normal. noted earlier. The reproductive system of
Blood lipid and blood calcium levels the male bird consists of a pair of testes,
also increase dramatically. However, ducts that carry the spermatozoa to the
even the increased levels of blood cal- cloaca, and in some species, an ejacu-
cium cannot provide enough resource to latory groove and phallus in the cloaca.
produce eggshell. Approximately 2000 Birds do not have the complement of
mg of calcium are needed to form the accessory glands that contribute the liq-
shell of a chicken egg. This represents uid portion of the semen in mammals.
about 100 mg per hour for the 20 hours Instead, seminal fluid is formed in the
the egg is present in the shell gland. tubules and ducts in the testes.
A 2 kg hen has a total of only 25 mg The testes are located ventral to the
of calcium circulating in her plasma. kidneys and just posterior to the adrenal
Thus, a laying hen must secrete approx- glands (fig. 10.2).3 These bean-shaped
imately four times more calcium into organs change in size as much as 300
the eggshell than is found in the blood. times from nonbreeding to breeding
This is accomplished by mobilizing cal- condition. It has been estimated that the
cium from specially formed reservoirs testes of a duck enlarge to almost 10%
of intramedullary bone. Many birds, of its body weight at the height of the
particularly species such as waterfowl breeding season. Generally, the left testis
that lay large clutches, rely on stored is larger than the right, although both
nutrients to successfully complete laying are functional. Within them, specialized
in as short a time as possible. Female germ cells called spermatogonia undergo
Lesser Snow Geese (Chen caerulescens) meiosis and cellular transformations to
accumulate fat reserves on their win- produce the spermatozoa, whose only job
tering ground in the southern United is to find and fertilize an ovum. Other
States and then migrate to the Arctic cells in the testes secrete androgens,
to breed before the snow melts. Their which influence development of second-
weight on arrival is still 20% above ary sexual characteristics associated with
normal. Females use their fat reserves the male and courtship behavior.
chapter 10

to produce eggs and to sustain them- Spermatozoa move from the tes-
selves during incubation. In fact, their tes to the cloaca via the highly coiled
reproductive success depends on their ductus deferens (or vas deferens). This

282

1stPages_B.indd 282 7/22/20 1:27 PM

 Anatomy and Physiology of Reproduction
Fig. 10.2. Urogenital organs of a House are sensitive to high temperatures in all
Sparrow (Passer domesticus) during breeding animals. In birds, this problem is often
(right) and nonbreeding seasons (Witschi solved by placing the sperm storage sac
1935). away from the body core in a cloacal
protuberance. Here, temperatures may
organ also increases greatly in size with be as much as 4°C lower than in the core,
breeding condition; in passerines, the which aids sperm survival.
sperm storage sac at the posterior end
of the ductus is about 100 times larger Copulation and fertilization
during breeding than during nonbreed-
ing. ­Spermatozoa that have moved down Copulation in birds consists of the trans-
the ductus remain in this storage sac fer of semen from the cloaca of the male
until the time of coition, when they are to the cloaca of the female. In most male
transferred to the female. Spermatozoa birds, only a very small, erectile phallus

283

1stPages_B.indd 283 7/22/20 11:46 AM

 occurs, and coition involves nothing of that found in other vertebrates.
more than close apposition of the cloacae Female birds produce two types of eggs,
of the two sexes. This “cloacal kiss” ones with a male sex chromosome and
usually takes just a few seconds, but it ones without. All sperm contain the
may last up to 25 minutes in the Aquatic male sex chromosome. The egg with a
Warbler (Acrocephalus paludicola) and male sex chromosome will produce a
90 minutes in the Greater Vasa Parrot male when fertilized; the egg without
(Coracopsis vasa) of Madagascar.4 In addi- the male sex chromosome will produce a
tion to the seasonal variation in testis female when fertilized. Thus, the female
size that occurs in all birds, there is often gamete is the one that determines the
variation within species in testis size sex of the offspring.
depending on social interactions and The sex organs of both male and
how these affect copulation frequency.5 female also contain several endocrine
In a few groups such as ratites, glands in the interstitial tissue sur-
tinamous, galliforms, and waterfowl, a rounding the germ cells that produce
fairly large, erectile, and grooved penis sex hormones that affect both devel-
aids in copulation. The structure of opment and behavior. We will discuss
this penis may be an important part of these further when we look at the timing
reproductive isolation between species, and synchronization of breeding events
as is the case in many insect species.6 (see below).
In the ostrich this organ may be as long
as 20 cm. Waterfowl use their penis for Egg Laying and Incubation
underwater copulation, such that the Egg laying
Lake Duck (Oxyura vittata) has a penis
that ranges from 20 cm to 42 cm. Once a female has reached the egg-lay-
Perhaps because of the relative inef- ing stage, an egg is laid each day in
ficiency of sperm transfer in most birds, most species until the clutch is com-
the semen contains a high concentration plete. Larger birds such as geese, swans,
of spermatozoa. It has been reported herons, hawks, and owls may lay eggs
that as many as 8.2 billion sperm per at about two-day intervals, while some
ejaculate are produced by some domes- species lay at even longer intervals.
tic roosters. Eagles and condors exhibit four- to five-
Once deposited within the female’s day intervals between eggs, and five to
cloaca, the semen may be stored in a sac seven days may elapse between the first
within the vagina. Although fertilization and second eggs of some seabirds. Most
may occur just several hours after cop- species lay their eggs in the morn-
ulation, in many species peak fertility ing, presumably because the shell has
occurs several days after copulation. formed and hardened overnight when
Because of their ability to store viable the female is not active, but there is a
sperm, females can remain fertile for great deal of variability in the time of
several weeks following copulation. One laying both within and among species.
chapter 10

event that occurs at the time of fertiliza- The number of eggs in a clutch
tion is sex determination. The sex deter- is also quite variable both within and
mination system of birds is the reverse among species. We will look at specific

284

1stPages_B.indd 284 7/22/20 11:46 AM

 reasons for this in chapter 12. Most tion provided by a nonparent, or even, as
species within a particular region exhibit in the case of the megapodes, by decaying
a typical clutch size, although this varies vegetation (see chapter 12). Developing
somewhat with age and time of nest- embryos are quite sensitive to fluctuating
ing. Young birds in general lay smaller temperatures, so the parent bird must
clutches than older birds, and first control the thermal environment of the
clutches during the breeding season are egg through various behavioral and phys-
generally larger than second clutches. iological adjustments.
For example, the Great Tit (Parus major) Optimal temperatures for develop-
has an average clutch size of 10 eggs ment in 37 species average 34°C. Tem-
in April nests, and only 7 eggs in June peratures above 43°C for just one hour
nests. are lethal for embryonic Heermann’s
The mechanisms that determine Gulls (Larus heermanni), and develop-
when a bird will stop laying and start ment of most avian embryos ceases
incubating are not fully known. Some below 25°C. Several studies have shown
species are determinate layers; that is, that the amount of incubation by the
a certain number of follicles mature parents is directly related to ambient
within the ovary with each breeding temperatures. In general, incubating
attempt, and once these have been laid, birds adjust the heat delivery to their
the clutch is complete, regardless of eggs by varying the time spent in direct
the number of eggs actually in the nest. contact with them, not by raising their
Other species are indeterminate layers, own heat production to warm the eggs.
because they have the capacity to keep To maintain egg temperature at about
laying eggs well beyond the number in 35°C, parental attentiveness (i.e., sitting
a typical clutch. Normally, these species on the eggs) increases with decreasing
must use visual or tactile cues in con- air temperature below 25°C and with
cert with hormonal adjustments to stop increasing air temperature above 35°C.
laying. If eggs are removed from the At air temperatures between 25° and
nest, though, they will lay eggs for long 35°C, parents allow the eggs to pas-
periods. Unfortunately, so much vari- sively heat or cool. The result of these
Anatomy and Physiology of Reproduction
ation occurs among birds that it is not adjustments is a surprisingly uniform
possible to classify all species as either thermal environment for the develop-
determinate or indeterminate layers. ing embryo (fig. 10.3).7 This is more
easily managed when both parents
Incubation share incubation responsibilities, so
that while one is on the nest, the other
When the clutch is completed, incuba- can leave to forage and rebuild its own
tion of the eggs commences. The heat energy stores. The eggs of single-sex
required to raise egg temperature to the incubators are much more likely to vary
optimal levels for embryonic develop- in temperature over the course of the
ment is usually provided by the parents day when the parent must leave the nest
through incubation. Little heat is pro- to forage. The amount of time spent
duced by the embryo, except at the end of incubating also varies with the stage
incubation. Only in rare cases is incuba- of development. Parental attentiveness

285

1stPages_B.indd 285 7/22/20 11:46 AM

 (as measured by the percentage of time to embryonic development than chill-
spent incubating) increases during the ing temperatures, and overheating by
first third of the incubation period in direct solar radiation of the nest can
Herring Gulls (Larus argentatus). In occur in any climate. Some species
this case, external heat supplied by the have developed means of regulating egg
parent plus the heat generated by the temperature under hot conditions. In
embryo itself helps maintain the embryo cases where external temperatures are
temperature between 37° and 38°C (fig. warm but not extreme, parent birds may
10.4).8 Only in larger birds do embryos not incubate but will simply shade or
generate more heat through growth late perhaps fan the eggs. In more extreme
in development than they lose through cases, though, the contact between the
evaporation, and consequently, less
incubation is required at this time. In
Fig. 10.3. Nest and egg temperatures (top)
smaller eggs, such as those of the House
from three different locations in the clutch (see
Wren (Troglodytes aedon), heat produced egg diagram) during the incubation period
by the embryo does little to elevate egg in the Herring Gull (Larus argentatus) and
temperature. how parental attentiveness is related to nest
Heat is probably more threatening temperatures (bottom) (Drent 1975).
chapter 10

286

1stPages_B.indd 286 7/22/20 11:46 AM

 Fig. 10.4. Contributions of parental and incubation (fig. 10.5).10 Interestingly,
embryonic heat to the regulation of egg these doves accomplish this without
temperature during incubation of Herring resorting to panting or gular flutter
Gulls (Larus argentatus) (O’Connor 1984). (see chapter 8); how they dissipate
heat during incubation is not known.
In extreme cases, a few open-habitat,
eggs and the incubating bird can cool ground-nesting species bring water
the eggs, or at least prevent them from to the eggs by wetting their feathers.
reaching a lethal temperature. Heat This both cools the nest and provides
from the egg is transferred to the parent, a moister environment for develop-
who dissipates it through radiative, con- ment. The Egyptian Plover (Pluvianus
Anatomy and Physiology of Reproduction
vective, or evaporative means. Studies aegyptius) incubates its eggs at night but
with the Double-banded Courser (Rhi- covers them with sand as the air warms
noptilus africanus), a ground nester of in the morning. During the heat of the
the Kalahari Desert of Africa, showed day it drops water onto the sand from its
that parent birds shaded but did not soaked ventral feathers, and evaporation
incubate eggs when temperatures were keeps the egg temperatures at about
between 30° and 36°C, but they used 37.5°C, compared to nearby sand tem-
constant incubation to maintain egg peratures of 46°C.11
temperature at air temperatures above In cold habitats, birds must incu-
36°C.9 Similarly, White-winged Doves bate continuously to maintain the
(Zenaida asiatica) nest in open desert large thermal gradient between egg
and, despite intense solar radiation and temperature and air temperature. Cold
air temperatures of up to 45°C, maintain climate creates energetic problems
egg temperatures at 39.2°C by constant for incubating adults because of their

287

1stPages_B.indd 287 7/22/20 11:46 AM

 Fig. 10.5. Variation in the air, egg, and brood from the surface of an incubating bird,
patch temperatures measured in an exposed may be as much as 10°C warmer than air
nest of the desert-dwelling White-winged Dove outside the nest. In some single-sex incu-
(Zenaida asiatica). In this species the brood bators, such as the Great Horned Owl
patch may be used to either heat or cool the (Bubo virginianus), which nests during
egg (Russell 1969). the middle of winter in the temperate
zone, the male brings food to the female
during both incubation and the early
restricted foraging time. Several adjust- nestling stages. Sometimes, however, the
ments are made by species that regularly parent is forced to abandon its eggs in
nest under these circumstances. Some order to forage at great distances from
species of hummingbirds, which are the nest, leaving the eggs to chill. Some
small, single-sex incubators, employ species of procellariforms, for example,
temporary hypothermia at night when neglect their eggs for hours or even days
ambient temperatures fall below 0°C. while they are foraging. Their embryos
This, of course, slows down embryo tend to be very resistant to chilling, but
development. Other small-bodied birds the effect of this intermittent incubation
circumvent the potential energy drain is reduced hatchability and a greatly pro-
of thermoregulation at night by utiliz- longed incubation period.
ing the nest microclimate to buffer the Incubation depends on intimate
decline in air temperature. contact between the incubating bird
The air temperature in nests placed and the eggs, so that the heat generated
chapter 10

in cavities, caves, or even within dense by the adult is passed to the eggs. This
conifers, which can greatly diminish the interaction can be viewed as though the
heat lost by radiation and convection eggs were simply an additional append-

288

1stPages_B.indd 288 7/22/20 11:47 AM

 age and the parent and eggs a single owls, while only the male has a brood
unit. The site of heat transfer between patch in phalaropes, jacanas, and some
parent and eggs is the incubation or sandpipers. In these latter cases, the
brood patch that is usually found on the brood patch of the male reflects a mat-
lower breast and abdomen of the bird. ing system in which the female defends
The area is generally characterized by a the territory and the male incubates; we
lack of feathers, edema leading to flabbi- will discuss this more fully in chap-
ness of the superficial skin and thick- ter 12. There is great variation in the
ening of the epidermis, and an increase occurrence of brood patches among the
in the number and size of blood vessels hawks and passerines; many species
and the musculature around these ves- have patches in both sexes, and in many
sels. All these modifications increase the others, only the female incubates. Much
efficiency of heat transfer between eggs of this variation may also reflect mating
and parent by allowing closer contact of and parental care characteristics. Only
the skin with the eggs and by increasing the pelecaniform seabirds, some of the
the amount of heat at the surface of the auklets, and the Bank Swallow (Riparia
well-vascularized brood patch. riparia) do not develop a brood patch.
In most species, the brood patch Many of these are burrow nesters, and
develops through the hormonal influ- the insulation properties of the bur-
ence of prolactin, which is secreted by row may preclude the need for a brood
the anterior pituitary gland, and estro- patch. At least some of the pelecaniform
gen, which is secreted by the ovary. species use their very large, webbed feet
Prolactin causes the defeathering of as the heat exchange organ in place of
the region, and estrogen produces the an abdominal brood patch.
epidermal thickening and vascular- Through the interaction of incuba-
ization. In many waterfowl the brood tion and the thermal environment pro-
patch is plucked by the bird, and the vided by the nest, the parents attempt to
downy feathers are then used to insulate provide the proper developmental envi-
the nest. In pigeons, the brood patch ronment for the eggs. At the same time,
occurs in a region without feathers (a through both properties of the nest and
Anatomy and Physiology of Reproduction
trait possible in part because all pigeons various behavioral patterns that we will
and doves have clutches of only one or discuss in chapter 11, the parents also
two eggs). In some species, the brood attempt to keep predators away from the
patch consists of distinct regions that eggs and nestlings.
are egg sized and arranged as the clutch
is arranged. For example, gulls have Egg Structure and
three distinct brood patches to match Embryonic Development
their typical three-egg clutches. In many
species both males and females develop Once an egg has been laid, the parents
brood patches to aid in incubation; are unable to provide any nutrients to
among these are the grebes, albatrosses the young bird until the egg hatches.
and relatives, pigeons, woodpeckers, How is the egg constructed so that it can
shorebirds, and cranes. Only the female provide the proper medium for develop-
has a brood patch in the galliforms and ment of a young bird? What can or (in

289

1stPages_B.indd 289 7/22/20 11:47 AM

 most cases) must the parents do to aid Yellow yolk is stratified in concentric
the proper development of the embryo layers around this core and is composed
within the egg until it hatches? How largely of lipoproteins and proteins
much variation occurs in egg develop- that are the main nutrient source of
ment and the final product, a baby bird? the embryo. The yolk mass makes up
As we attempt to answer these ques- 20%–65% of the egg, depending in part
tions, we must remember that a bird egg on the type of development (altricial or
starts out as a single cell composed of precocial).
all the appropriate nutrients needed for Surrounding the yolk are the
development but with very little struc- “whites,” or albumen. Albumen makes
ture. The process of growth within the up about 65% of the egg mass in pre-
egg consists largely of the incorporation cocial species and is composed entirely
of these nutrients into the embryo. of protein and water. It is arranged
into three compartments. Immediately
Egg structure surrounding the yolk is the chalazif-
erous layer, a thick, viscous layer that
Since the whole purpose of an egg is forms twisted fibrous strands (chalazae)
the production of a young bird, let us that anchor the yolk to the poles on
start our look at egg structure with the long axis of the egg. Next is a thin,
the embryo. When the egg is laid, the watery inner layer of albumen around
embryo is a tiny spot called the germinal the yolk, and then a middle layer that
disc, which sits on top of the yolk mass
(fig. 10.6). The embryo remains at this Fig. 10.6. Summary of development within the
location even when the egg is moved, egg, including the structure of the egg before
because the yolk floats freely within incubation (left) (Romanoff and Romanoff
the egg. The yolk of a chicken egg has 1949), the general patterns of embryonic
a definite structural organization. A membranes and circulation during development
whitish layer of yolk within the center (middle) (Patten 1951), and the position of a
of the mass is highly proteinaceous. bird at the time of hatching (right).

1stPages_B.indd 290 7/22/20 11:47 AM

 is much thicker and more viscous, and (CaCO3). This mineral is arranged in ver-
finally a thin, watery outer layer. The tical columns, between which are minute
differences in the various layers lie air spaces that open to the surface as oval
only in the amount of water or fibrous or circular pores (fig. 10.7). There are
ovomucin protein they contain. The thousands of these minute pores over
yolk is suspended in these layers of the surface of the shell; estimates range
albumen yet is anchored so that, as the from 6,000 to 17,000 in a chicken egg.
egg rotates, the embryo stays on top of Apparently, these pores function in gas
the yolk. The albumen is also important exchange; studies have shown that the
for several other reasons: it provides an number and sizes of pores vary with alti-
aqueous environment for development, tude and climatic conditions.12 The pore
it retards desiccation, it has antibacterial size and density greatly influence the
properties, and it provides an additional rate of gas exchange (O2, CO2, and water
nutrient source for the embryo. vapor) across the eggshell and are a mea-
Surrounding the albumen are sure of the shell’s conductance or diffu-
two fibrous shell membranes made sivity. Eggs laid under humid or hypoxic
of another protein, keratin. The inner (low O2) conditions, such as in burrows
membrane rests on the surface of the or under vegetation (as in megapodes),
albumen and holds this watery layer of often have elevated conductance in
the egg together. The outer layer is about order to facilitate movement of O2 to the
three times thicker and has elements of embryo and CO2 from the embryo. The
the external shell anchored in it. The two greater potential for water loss from the
layers separate at the blunt end of the egg is not realized in this case because
egg, where they create an air space that of the higher humidity surrounding the
enlarges during development, as yolk is egg.
absorbed by the embryo, and provides The outermost covering of the egg
the first air to the baby bird just prior to is the cuticle, which imparts the charac-
hatching. teristic surface texture of the egg. The
The calcareous shell is the external adaptive significance of the various outer
barrier, and it serves a variety of func- coverings of eggs (glossy, greasy, chalky,
Anatomy and Physiology of Reproduction
tions that require some compromises in ridged, powdery) is not known. The cuti-
structure. For example, the shell should cle has been most thoroughly examined
be hard enough to keep the egg from in chickens, in which it is a thin, contin-
breaking easily under the weight of the uous layer of glycoprotein over the entire
incubating parent, but not too hard for shell, including the pores. It imparts
the hatchling to break through. It must water-repellent properties to the egg’s
be porous enough for diffusion of oxy- surface and impedes both water loss
gen into the egg and carbon dioxide out through the shell and bacterial entry.
of it, but not so porous that the embryo All the above structures result in an egg
desiccates or that bacteria can enter the that is, at the time of laying, about 65%
egg. To accomplish all this, an organic water, 12% protein, 10% lipid, and 11%
(protein) framework serves as a skeleton mineral.
for deposition of inorganic minerals, Egg size and shape vary with the
98% of which are crystalline calcite type of bird. The largest egg we know of

291

1stPages_B.indd 291 7/22/20 11:47 AM

 Fig. 10.7. Structure of the avian eggshell and of the bird (table 10.1). For example, an
location of the pores. ostrich lays an egg that is about 1.8% of
its body weight, while a wren lays one
that approaches 14% of its weight. Many
was that of the Elephant Bird (Aepyornis exceptions to this general trend occur,
maxima) of Madagascar, which had a though. For example, the kiwi lays an
capacity of more than 9 L and mea- egg that is about 18% of its body weight,
sured 34 cm by 24 cm. The smallest egg rather than the 3% expected for a bird
known is that of a hummingbird, the of that size. Birds lay larger eggs as
Jamaican Emerald (Mellisuga minima); they get older, and the eggs of precocial
the egg is only 1 cm by 0.65 cm, and species are usually larger (10%–15% of
its mass is 0.5 g, or about 1/​50,000 the the female’s body weight) than those of
mass of an Elephant Bird egg. Many similar-sized altricial species (5% of the
factors influence the size of bird eggs. female’s weight).
chapter 10

Generally, larger birds lay larger eggs, Generally, eggs are semielliptical,
but the size of the egg relative to its with one pole slightly flattened and the
parent decreases with increasing size other more pointed, but some variation

292

1stPages_B.indd 292 7/22/20 11:47 AM

 Table 10.1
Egg weight as a proportion of female body weight
species adult female egg weight (g) egg weight/body
body weight (g) weight (%)
Ostrich 90,000 1600 1.8
Emperor Penguin 30,000 450 1.5

Mute Swan 9000 340 3.8

Snowy Owl 2000 83 4.1
Peregrine Falcon 1100 52 4.7
Mallard 1000 54 5.4
Herring Gull 895 82 9.2

Puffin 500 65 13.0

Robin 100 8 8.0

House Sparrow 30 3 10.0

House Wren 9 1.3 13.7

Vervain 2 0.2 10.0
Hummingbird
Source: Perrins and Birkhead, 1983.
Note: Both egg weights and female body weights are approximate.

in shape does occur.13 Birds that nest on colors are merely a means of excreting
the ground or on cliffs often have eggs metabolic waste products, it is more
that are quite pointed and pear shaped likely that their primary function is a
Anatomy and Physiology of Reproduction
(pyriform); this shape allows the eggs to protective one, to camouflage the eggs
be packed tightly together during incu- and to shield the developing embryos
bation and produces a very tight circle from incident ultraviolet radiation.
when they are rolled. Consequently, Support for the latter view comes from
when the eggs are moved, they do not go the white eggs of hole-nesting species,
very far. Some birds, particularly cavity which typically experience lower pre-
nesters, lay eggs that are nearly spheri- dation and little to no incident solar radi-
cal. The shape of the eggs is most likely ation. The color and pattern of markings
related to the pelvic structure; the deeper on the eggs of the Common Murre (Uria
the pelvis, the more spherical the eggs. aalge; fig. 10.8) are extremely variable
Eggs are quite variable in texture and may aid the parent in locating its
because of differences in their cuticle single egg within the densely populated
layer. Egg color is also highly variable. nesting colony on rocky ledges. It has
While it has been suggested that these been proposed that the brightly colored

293

1stPages_B.indd 293 7/22/20 11:47 AM

 eggs of the tinamou allow the parents Fig. 10.8. Variation in eggshell color in a single
to find all the eggs after they have been species, the Common Murre (Uria aalge).
protectively camouflaged with leaf
­litter.14 However, one of the main ben-
efits of egg color is protection against etration of the sperm. The male and
predation, accomplished by camouflage. female pronuclei fuse to the zygote
For example, it has been suggested that nucleus, and the first cleavage division
blue eggs in dark nests that are placed occurs three to five hours after fertil-
in isolated areas receiving partial sun ization while the egg is in the magnum
seem to imitate the spots of light on and the inner layer of albumen is being
green leaves in a forest. Buff-colored added. The second cleavage division
eggs occur in birds that lay them in coincides with the laying down of the
leaf litter or on other dull but well-lit shell membranes in the isthmus. By the
substrates. White-spotted eggs occur in time the egg reaches the uterus, it has
thinly formed nests in poorly lit, sparse reached the 16-cell stage, and when it is
foliage, where the egg tends to vanish laid, the embryo consists of a double-lay-
against its speckled background. It has ered blastula oriented at right angles to
recently been suggested that egg color is the long axis of the egg. In most cases,
a measure of egg quality, such that indi- embryonic development is suspended
viduals that lay brightly colored eggs are after an egg is laid, and then it resumes
showing their good physical condition. with the regular application of heat to
the egg through incubation. It is beyond
Embryonic development the scope of this book to examine the
many details of embryonic development,
The development of the embryo begins but we do want to look at general pat-
chapter 10

with cell divisions almost immediately terns of development and the require-
after fertilization. The second meiotic ments for them.
division of the ovum occurs after pen- Early in its development, the embryo

294

1stPages_B.indd 294 7/22/20 11:48 AM

 becomes enveloped in the amniotic from the saturated interior of the egg
layer, which forms a fluidfilled cham- to the less humid microclimate of the
ber around it and protects it. Next, cells nest must also be regulated. Variation in
grow downward and envelop the yolk, the construction of the eggshell among
forming a yolk sac; veins develop on the species enables all avian embryos to be
surface of the yolk sac that transport exposed to roughly the same conditions.
nutrients from the yolk to the embryo. In fact, experiments on domestic fowl
Shortly before hatching, the yolk sac is have shown that O2 levels less than 15%
drawn into the body so that stored nutri- or greater that 40% (normal is 21% of
ents are still available after hatching. In atmospheric air) or CO2 levels greater
many species, hatchlings can live for than 1% (normal is 0.03%) greatly
several days on stored reserves from the retard embryonic development. As a
yolk. Finally, in the early development consequence, despite large variations in
of the embryo a third membrane devel- egg mass, incubation period, climate,
ops, the allantois (fig. 10.6; also called geography, and so forth, avian embryos
the chorioallantois). This grows out as a complete their development with similar
pouch from the hindgut to line the inner water losses (about 16% of the initial egg
surface of the shell membrane, where mass), similar amounts of O2 consumed
it serves as both a bladder, or waste per gram of embryo, similar gas pres-
depository, and a respiratory organ. A sure gradients across the shell, and sim-
rich supply of blood vessels develops in ilar O2 and CO2 content in the air cell
the allantois near the shell and facili- before hatching.15 Hatchability depends
tates gas exchange. The allantois also on the consistency of these parameters
serves as a depository for nitrogenous during development.
wastes, generally in the form of uric Development also requires parental
acid salts. By excreting uric acid into the (or other) input of external heat energy
allantois, the avian embryo can avoid to maintain egg temperature at an opti-
the potential toxicity of accumulated mal 37°–38°C (see discussion of incu-
nitrogenous waste and conserve water bation above). We have pointed out that
at the same time. (See the discussion of temperature tolerances of embryonic
Anatomy and Physiology of Reproduction
water conservation by uric acid excretion development are rather narrow, and it
in chapter 2.) The uric acid salts form should be noted that the optimal devel-
crystals, which are simply stored outside opmental temperature is very close to
the embryo until hatching. the lethal temperature for avian embryos
The optimal development of an (above 43°C). In addition, tolerance to
embryo requires the appropriate gaseous temperature extremes declines with
environment, an external source of heat, development; embryos close to hatching
and the proper egg position, including, cannot stand the extremes that a freshly
in most cases, turning of the egg. The laid egg can.
gaseous environment is controlled by Parents must not only provide
gas exchanged through eggshell pores. the heat for incubation but must also
The outward diffusion of CO2 and manipulate the eggs so that each
inward diffusion of O2 is of primary receives uniform heat. A tempera-
importance; movement of water vapor ture gradient of as much as 5.6°C was

295

1stPages_B.indd 295 7/22/20 11:48 AM

 measured between the central and birds exhibit some ecological adjustment
peripheral eggs in the clutch of the of embryonic development, such that
Mallard (Anas platyrhynchos).16 Turning open-nesting birds have shorter develop-
the eggs is also important to prevent ment times than hole nesters. This may
adhesion of the membranes to the shell occur because of the higher predation
early in development. Repositioning pressures on open nesters, and the need
of eggs also aids the development of to hurry the developmental as well as the
their equilibrium position. At first, the subsequent nestling growth process.
yolk mass is free to revolve in the shell
and the embryo remains uppermost Hatching
because it floats on a lighter portion of
the yolk. Later, however, the extraem- Hatching is obviously a critical stage in
bryonic membranes fuse with the shell the development of a baby bird, for it
membranes, and the embryo position involves escape from the confinement
becomes fixed in the shell with the head of the shell and conversion from the
oriented toward the blunt pole and the embryonic to adult form of such phys-
air space. The egg then becomes asym- iological processes as breathing, excre-
metric in weight and will always assume tion, and so forth. The shift between
a certain orientation, with embryo functional systems must be done fairly
uppermost, when it is rolled in the nest. quickly.
The time required for embryonic Hatching success is highly depen-
development is variable, even among dent on the proper position of the
birds of similar size and taxonomic affil- embryo within the egg. During the days
iation. Generally, large birds lay larger before hatching, the embryo assumes
eggs and have longer development times what is known as the “tuck” position,
than small birds.17 However, other fac- with the head between the right wing
tors affect the length of incubation and and the body with the bill pointed
embryonic development. Young birds toward the blunt end of the egg (fig.
at hatching are not equivalent develop- 10.6). From this position, the first act
mentally. Woodpeckers, for example, of hatching involves puncturing the air
hatch at an early stage compared to sac and the initiation of lung breathing
small passerines, and although their by the embryo. This stage occurs a day
development time would appear short, or two before actual hatching. Pipping,
they are not as mature as other altricial or shell breakage, also occurs from this
nestlings with longer development. The position. The first pip may occur 10
same is true in comparisons of preco- hours or more before hatching as the
cial and altricial young. Precocial young result of a random movement of the
have much longer development times embryo. At some point, this movement
than altricial young do, but their organ becomes much more active and involves
systems are much better developed, and strong thrusts of the beak into the shell,
they can essentially feed and take care accompanied by propulsive movements
chapter 10

of themselves soon after hatching (see of the entire body by pushing with the
the section on nestling development feet. In the process, the embryo rotates
below). It has also been suggested that within the shell, causing a ring of cracks

296

1stPages_B.indd 296 7/22/20 11:48 AM

 near the blunt end. This process is aided over a span of 16 hours. In the wild, a
by specialized structures in the full- clutch of Mallard eggs usually hatches
term embryo: a horny knob or egg tooth over a period of only two to eight hours.
on the upper mandible, and hatching The male Rhea (Rhea americana) incu-
muscles on the back of the head that are bates the eggs of several females, and
responsible for the vigorous back thrust although eggs may be deposited in a
of the head during pipping (fig. 10.9).18 nest over a two-week period, or even
Both structures either fall off or regress added after incubation is started, the
shortly after hatching. Usually one entire clutch usually hatches within
rotation within the egg will result in a two to three hours. It is obvious from
severing of the cap of the egg, although these observations that some sort of
two or three rotations have been behavioral modification by the embryos
observed in some birds. Eventually, the synchronizes the final hatching process.
embryo will break off the cap and the Studies of how this might be accom-
thrusting motion will push the baby bird plished have focused on gallinaceous
out of the shell, but this may take several birds and waterfowl, where the hatching
hours, or even several days in albatross synchrony is critical because the parents
chicks. lead the young from the nest soon after
Embryonic development is a series hatching. All young birds emit a clicking
of chemical processes whose rates are a noise just prior to hatching and shortly
function of the external heat provided. after they develop the ability to breathe.
However, if heat were the only factor The clicking apparently synchronizes
that affected development, variation the hatch by speeding up the final devel-
in hatching times of eggs in a clutch opment of nestlings that are somewhat
would be expected to reflect differences behind in the hatching process and
in their laying times. This is not the perhaps by retarding the movements
case. For example, eggs taken from a
Mallard nest shortly after completion of
the clutch were incubated and hatched Fig. 10.9. Hatching muscle and egg tooth of
a chicken on the day of hatching (Bock and
Anatomy and Physiology of Reproduction
Hikida 1968).

297

1stPages_B.indd 297 7/22/20 11:48 AM

 of the more advanced individuals.19 Fig. 10.10. Simple overview of the hatching
Thus, through acoustic communication types, their traits upon hatching, and their
between the embryos, hatching occurs variation in egg composition. The most
in a minimal time. altricial type is shown at the top and the most
precocial at the bottom (Ricklefs 1983; Ar,
Ariels, Belinsky, and Yom Tov 1987).
Stage of development at hatching

Up to this point, we have looked at a

general pattern of development, but Hatched birds have been classified
most everyone knows that baby chickens into several developmental categories.
are different from baby robins in how Precocial young are those that hatch with
they behave and in the amount and type their eyes open, are covered with down,
of care they require. While baby chicks and can leave the nest in a matter of a
or ducks may be good pets for children, few hours or a day or two (fig. 10.10).
one would not want to give a child a Some precocial chicks grow up inde-
clutch of recently hatched robins or pendently of their parents, but others fol-
chapter 10

bluebirds as pets! Obviously, the extent low their parents (walking and/​or swim-
of development during incubation varies ming), who either feed them or show
among birds. them food. Ducks, chickens, grebes, and

298

1stPages_B.indd 298 7/22/20 11:48 AM

 many sandpipers have precocial young; tems that allow even a new hatchling to
they are also described as nidifugous, or stand immediately, to run from preda-
nest fugitives, for their behavior of leav- tors, and to seek its own food.
ing the nest. Altricial birds are those at
the other extreme; they hatch with their Nestling Development
eyes closed, have little or no feathering, Growth of altricial versus
and require great amounts of care and precocial nestlings
feeding (fig. 10.10). Most passerines and
other small birds fit into this category; Most young birds grow rapidly at first,
these young are also termed nidicolous, but their growth rate slows as they
or nest dwellers, because of their pro- approach adult size. The pattern for most
longed occupancy of the nest. birds is a sigmoidal growth curve (fig.
Within these groups, two other 10.11).21 Although the shape of the curve
categories are regularly recognized (fig. and the actual daily growth rates may
10.10).20 Semiprecocial birds hatch vary greatly between species, this is a
with their eyes open and have a downy consistent pattern of growth in all birds.
covering, but although they are able to The gradual diversion of food energy
walk, they do not leave the nest and are from primarily growth to maintenance
generally fed by their parents. Included and activity during development is the
among these are gulls and terns. Semial- basis for the sigmoidal shape of the
tricial birds are somewhat less developed growth curve. To illustrate this point, we
than the above; they are down covered will describe some characteristic features
but are not able to leave the nest. The of the nestling development of altricial
semialtricial nestlings of hawks and young and compare their development
herons hatch with their eyes open, while with that of precocial young.
those of owls have their eyes closed. After hatching, altricial nestlings
The difference in the product that are totally dependent on their parents
hatches obviously reflects differences in for food and for maintaining their body
egg composition between precocial and temperature. During the first third of
altricial birds; eggs of precocial young the nestling period, the young move
Anatomy and Physiology of Reproduction
often have larger yolks than those of about very little but begin to have better
altricial young, and much of the yolk control of their head and neck; feathers
remains at hatching as an internalized emerge and begin to grow but the body
yolk sac. More important, however, is is still largely devoid of insulation. The
how growth is apportioned to the vari- nestlings have little control of their body
ous organs of the body during embry- temperature when exposed to cold at this
onic development of precocial and altri- early stage. Because most of the energy
cial young. Altricial nestlings hatch with ingested goes into building tissue, the
still relatively immature organ systems. young can achieve very high growth
Only the digestive tract is well developed rates. During the next third of the nest-
at hatching, enabling them to maximize ling period, feathers cover more of the
their assimilation of food. In contrast, bare skin and the young begin to shiver
the precocial hatchling is a miniature and move around in the nest. With better
adult with relatively mature organ sys- insulation and more heat production

299

1stPages_B.indd 299 7/22/20 11:48 AM

 from the musculature, the young now Fig. 10.11. A comparison of growth curves of
exhibit better control of body tempera- young from several species of birds. Note that
ture during cold exposure. They are alert some exceed the weight of their parents while
to external cues and exhibit appropriate in the nest, while others fledge when lighter
innate behaviors (e.g., begging from than their parents (O’Connor 1984).
the parent, crouching in fear). During
the final third of nestling development,
feather development is completed, tem- altricial nestlings. As we have discussed,
perature and sensory responses become precocial young can walk, see, and feed
acute, and the young exercise in the nest, themselves soon after hatching. They are
preparing themselves for flight. More also able to thermoregulate within limits.
intensive foraging efforts by the parents This means that they must allocate more
for these large and voracious nestlings of their daily energy to maintenance and
mean that the young must expend more less to growth; the further development
energy regulating their own body tem- of their relatively advanced organ sys-
perature. Consequently, the ingested tems leaves even less energy for overall
energy channeled into growth decreases growth. Finally, these young must move
and the growth rate slows. Increased around to feed and to escape predation,
activity of older nestlings is another and some energy must be diverted away
source of energy diversion away from from growth and into activity costs.
growth, but most nestlings are close to The marked differences in develop-
adult size at this time. mental rates between altricial and preco-
chapter 10

Although the growth curve of pre- cial nestlings suggest two major options
cocial nestlings is sigmoidal, the growth in reproductive strategies among birds.
rate is only about one-third that of Those with altricial young can produce

300

1stPages_B.indd 300 7/22/20 11:48 AM

 offspring rather rapidly because of their diet and food availability, predator
high growth rates, but these young pressure, climate, internal allocation
require extensive amounts of care, of energy, even biochemical processes.
including brooding to keep them warm, Generally, small birds grow more
and must be provisioned with high-en- quickly than large ones, young in open
ergy foods. This strategy also carries a nests grow faster than those in cavities,
higher risk of predation, and the parent temperate zone birds mature faster
risks losing all its reproductive invest- than their tropical counterparts, species
ment during the nesting period. at high altitudes mature faster than
In contrast, precocial young are at those at sea level, and young fed insects
risk from predation only during the develop more quickly than those fed a
incubation period, because nestlings can fruit diet.
usually avoid predators from the time Explanations for the intraspecific
of hatching on, and rarely are whole variation in growth rates among young
clutches lost. Precocial young do not birds have focused on several of these
require as much care as altricial young, constraints. British ornithologist David
since they often need only to be guided Lack (1968) regarded growth rate as
to appropriate feeding locations and a balance between predation pressure
protected (often just through warn- selecting for rapid growth and food
ing) from predators. The primary cost supply selecting for slower growth. Lack
in such a seemingly easy strategy is a proposed that young birds exposed to
longer nestling development period than high risk of predation should grow as
that of altricial young; as a consequence, fast as possible to outgrow this possible
it is more difficult to rear more than one mortality factor. The Lack hypothesis is
brood per breeding season. Young pre- supported by the slower growth rates
cocial birds require access to prey that is found in hole or cavity nesters (low
fairly easy to capture, but their reduced predation pressure) compared to those
growth rates also mean that they can in open-nesting birds (high predation
survive on somewhat lower-quality foods pressure) in similar areas. In addition,
than altricial young. The above factors Lack hypothesized that the growth rate
Anatomy and Physiology of Reproduction
tend to release the parents from some of the young is adjusted to the food the
of the constraints of care that are related parents can provide. A slower growth
to the number of young, so that birds rate in hole nesters means that less food
with precocial young tend to lay larger is required per young per day, which in
numbers of eggs in a clutch (see the turn implies that parents can therefore
discussion in chapter 12 on the limits of raise larger broods of young. In fact,
clutch size). hole nesters do have larger broods.
Other groups exhibiting slow growth
Factors affecting growth rate include those that live on predator-free
islands and those whose young can run
After baby birds hatch, their develop- away from predators, all of which sup-
ment depends on various features of port the Lack hypothesis.
parental care and a set of external and American ornithologist Robert Rick-
internal constraints that limit growth: lefs (1969) was not convinced by Lack’s

301

1stPages_B.indd 301 7/22/20 11:48 AM

 arguments and retested the hypothesis diet of young petrels fed an oily regurgi-
that growth rates were optimized by tant by their parents has been proposed
mortality patterns of each species. A as one of the reasons for their slow
clear correlation between growth rate growth. However, parental choice of
and mortality was absent in the many highly nutritious items for their young
species he examined. Ricklefs further should generally rule out the nutrition
countered that food requirements do hypothesis for all but a few species
not increase proportional to increases in Organismal constraints on growth
growth rate. For example, doubling the rate may be set by the young bird’s
growth rate of the slow-growing Leach’s ability to assimilate the ingested food.
Storm-petrel (Oceanodroma leucorhoa) The size of the digestive tract is propor-
would increase the energy required for tionally larger and is more mature in
growth by only 5%. altricial young than in precocial young.
The Lack hypothesis also does not This disparity of development between
explain why most tropical birds with the two groups leads to the conclusion
high nest predation have slower growth that altricial young can assimilate more
rates than their temperate counterparts energy and thus can grow faster than
with comparatively lower nest predation. precocial young. Feeding experiments
Lower metabolic rates of tropical species with Blue Tits (Parus caeruleus) also
and the lower nutritional quality of their support this hypothesis.22 To demon-
diet could be responsible. In fact, trop- strate that the slower growth of late
ical birds that feed their young fruits, broods of this species was related to the
which may be of poor nutritional quality, high concentration of oak leaf tannins in
tend to have slow-growing offspring their prey, Chris Perrins compared the
(table 10.2). In contrast, nestlings fed growth rates of young reared on plain
highly nutritious food, such as insects, mealworms with those of young fed
grow more rapidly. The protein-deficient mealworms contaminated with tannic

Table 10.2
Growth rates of Neotropical birds in relation to nestling diet
Growth Constant

diet range mean ± sd (n)

Fruit 0.098–0.460 0.262 ± 0.151 (5)
Mixed fruit-insect, mostly fruit 0.280–0.464 0.375 ± 0.076 (6)
Mixed fruit-insect, mostly insect 0.199–0.536 0.379 ± 0.102 (9)
Insect 0.236–0.524 0.375 ± 0.078 (13)
Nectar-insect 0.256–0.362 0.317 ± 0.055 (3)
chapter 10

Seed 0.472–0.520 0.496 ± 0.034 (2)

Source: Ricklefs, 1983.
Note: Rate constants of the logistic equations are fitted to the growth data.
302

1stPages_B.indd 302 7/22/20 11:48 AM

 acid. The uncontaminated young gained shortly after the young leave the nest,
weight faster and exhibited more intense but in some species the parents provide
begging activity and interest in food. care for up to three weeks postfledging.24
Ricklefs has proposed that two At the time of true independence from
types of physiological constraints limit their young, parents may refuse to feed a
growth rates of birds. Biochemical and begging youngster, forcing it to look for
molecular constraints limit the extent food itself. Eventually the young learn to
to which functionally mature tissue can follow the adults and search where they
continue to grow and proliferate. Thus, are feeding, until finally they become
growth rates are determined by a bal- completely independent. In some spe-
ance between the mature and embryonic cies, such as blackbirds and sparrows,
functions of tissues.23 Generally, growth large flocks of young birds form at the
and differentiation are two competing end of the breeding season; they roost
and mutually exclusive processes in together and may migrate together, sepa-
tissue development. That is, maturation rately from their parents.
of nerve and muscle tissue into a more However, in some owls, the fledg-
refined locomotory system cannot be ling period is prolonged for months, as
accomplished while muscles are grow- the young learn where and how to find
ing larger and developing neuronal their food under limited light conditions.
connections. This explains why growth Birds receiving extended parental care
slows as tissue matures and also why, probably benefit either from avoiding
in altricial young, we first see a rapid food shortages while still inexperienced,
growth phase, followed by a maturation or from learning how to forage. (Parental
phase of slower growth. behavior during the fledgling period is
The second physiological constraint discussed further in chapter 11.)
is a consequence of tissue maturation.
Mature organ systems have higher The Timing of Reproductive Events
maintenance costs, and a greater per-
centage of the assimilated energy must In an evolutionary sense, birds should
be diverted away from growth into breed at the time when they can produce
Anatomy and Physiology of Reproduction
maintenance. Similarly, on an organis- the most offspring that can survive to
mal level, as the young mature, more of breed in the future. In the temperate
their assimilated energy is diverted into zone, this is usually during the spring or
thermoregulation and activity, leaving summer, when temperatures are mod-
less for growth. erate and food is abundant. Even in the
tropics, the wet-dry seasonal cycles affect
Fledging nesting seasons. Rather than focus here
on the ultimate, evolutionary factors
Growth and development generally stop affecting the timing of nesting (many
when the offspring reaches adult size. of which we will discuss later), we will
In most species, at or near this point address the proximate factors that deter-
fledging occurs, in which the young bird mine breeding time. Given that evolu-
leaves the nest, learns to fly, and fends for tion mandates that June, for instance, is
itself. Parental care may be terminated the time to nest, how do birds synchro-

303

1stPages_B.indd 303 7/22/20 11:48 AM

 nize the many changes necessary to ini- To use day length to regulate repro-
tiate the breeding process and advance ductive function, birds must have photo-
from one stage of reproductive behavior receptors and some means of measuring
to the next? time. The eyes are the most logical pho-
The synchronization of the stages toreceptor, but many investigators have
in the reproductive cycle is complex. demonstrated that the eyes are not essen-
Initiation and termination of one stage tial, at least in testicular development. In
are requisite for proceeding to the next: a classic experiment, researchers used a
arrival of spring migrants is followed by quartz rod to direct light of various wave-
establishment of territory, which leads to lengths directly to the brain of blinded
courtship of the female, ovulation, com- Mallards and found that the maximal
pletion of the clutch, incubation, and so testicular growth occurred with red light
forth. This sequencing is rather rigid in directed toward the hypothalamus.26 In
birds; that is, individuals at one hor- fact, the hypothalamus was 100 times
monal stage in the cycle may be unre- more sensitive to photostimulation than
sponsive to external stimuli associated was the retina. Other researchers have
with another stage. For example, during used luminescent beads or optic fibers to
the nest-building stage, adults may be deliver light to selected areas within the
completely unresponsive to the begging brain and have found that stimulation
stimuli of nestlings placed in their nest. of the ventromedial hypothalamus with
light produced the greatest response of
Photoperiod control of reproduction gonadal (testis) growth.
The existence of a biological clock
In the temperate zone, the external cue for measuring day length, or even
that most often initiates the develop- longer periods of time up to a year, has
ment of the reproductive organs and the been documented for both plants and
start of the breeding process is increas- animals, beginning with Erwin Bun-
ing photoperiod; that is, an increase in ning’s experiments in the 1930s.27 The
the amount of light each day. Factors structures included in the clock are
such as rainfall, social conditions, or the pineal gland, the suprachiasmatic
food supply may also affect the initia- nucleus (located in the hypothalamus
tion of breeding, but these often serve above the optic chiasm), and perhaps
as final cues for the fine-tuning of the the retina as well. The biological clock is
reproductive response. In some species, responsible for maintaining the internal
however, these factors may be the pri- (endogenous) daily (circadian) rhythms
mary cues used to initiate reproduction. of hormonal cycles, body temperature
For example, in the Red-billed Quelea cycles, metabolic activity, locomotor
Finch (Quelea quelea), rainfall and green activity, and so forth. To prevent the
vegetation seem to be the proximate daily rhythms from becoming out of
inductive factors.25 These birds migrate phase with the real world, the clock is
across Africa following the rains and “entrained” to an external cue (zeitgeber),
chapter 10

stop to breed wherever and whenever such as light. In the absence of light, the
the females can store enough energy clock may be entrained to sound, or to a
reserve to produce a clutch of eggs. number of other peripheral cues that act

304

1stPages_B.indd 304 7/22/20 11:48 AM

 as time cues. Thus, sparrows entrained under 12-, 36-, and 60-hour regimes had
to a light-dark cycle will continue a par- large testes, while birds kept under 24-
ticular rhythm of body temperature, for (the control), 48-, and 72-hour regimes
example, when maintained in constant had testes of the normal immature size.
darkness. Without the light cue each The daily photoinducible phase contin-
day, however, the temperature rhythm ued to oscillate in birds kept in darkness
assumes the periodicity of the biological for as long as 66 hours (the 72-hour
clock (usually somewhat longer than 24 regime). The reason that gonadal growth
hours) and becomes asynchronous with occurred in the 12-, 36-, and 60-hour
real time. It was found that removal of treatments was that the 6-hour light
the pineal gland (a small appendage of period occurred during the photoinduc-
neural tissue near the dorsal surface of ible phase. When the light occurred only
the brain) caused the activity of sparrows during the first half of the cycle, there
kept in constant darkness to be sporadic, was no stimulation.
with no periodicity at all. The pineal The internal coincidence model
gland secretes a hormone called mela- assumes that changes in photoperiod
tonin, which can affect the secretion or will cause changes in the temporal rela-
action of other brain hormones. Even in tionship between two or more circadian
culture and in darkness, the pineal gland rhythms. A specific temporal relation-
releases melatonin rhythmically, with ship between the two rhythms induces
peaks occurring about every 24 hours. the physiological process. For example,
In addition to the endogenous circa- it was found that injection of prolactin
dian rhythms already mentioned, there 12 hours after the daily rise of plasma
is a circadian rhythm of photosensitivity. corticosterone promoted fattening,
A particular physiological event may be gonadal growth, and northward-oriented
induced when light is received during migratory restlessness in White-throated
the photosensitive period. Based on this, Sparrows (Zonotrichia albicollis), all char-
it is easy to see how changing day length acteristic of a spring-breeding bird.29 In
might initiate the entire cascading series contrast, injection of prolactin 8 hours
of events in the reproductive cycle. after the rise in corticosterone in these
Anatomy and Physiology of Reproduction
At present there are two theories that birds resulted in no fattening or catab-
explain how light induces reproduction. olism of fat, no gonadal growth, and no
The external coincidence model migratory restlessness, which is more
states that gonadotropin release, for typical of a midsummer-breeding bird.
example, occurs when light is coincident The two coincidence models are not
with the photoinducible phase of the mutually exclusive, but both are useful
daily cycle. Researchers exposed photo- in understanding the initiation of repro-
sensitive male House Finches (Carpo- ductive events, because some of the
dacus mexicanus) to light-dark cycles of processes seem to be better explained by
varying length to test this model.28 The one model and other processes by the
duration of light in these experiments other model.
was always 6 hours, but the total length The amount of day length neces-
of the cycles ranged from 12 to 72 hours. sary to stimulate gonadal growth differs
At the end of the experiment, birds kept greatly among species, but in general,

305

1stPages_B.indd 305 7/22/20 11:48 AM

 the day length required to photostim- interstitial tissue (Leydig cells) secretes
ulate is about the same as that experi- testosterone; in the female, the gran-
enced at the breeding site. For example, ulosa and thecal cells that surround
there is a direct relationship between the ovum secrete progesterone and
critical day length and latitude of breed- estrogens, respectively. These steroids
ing in swans. Bewick’s Swan (Cygnus circulate through the blood to the
columbianus), which breeds at 65° N secondary sex organs (e.g., the oviduct
latitude, requires 16.5 hours of light of the female or the vas deferens of
for photostimulation; the Mute Swan the male) and are responsible for the
(Cygnus olor), which breeds at 55° N growth, vascularity, and secretory nature
latitude, requires 14.5 hours of light; and of these structures during reproduction.
the Black Swan (Cygnus atratus), which They also circulate back to the brain,
breeds at 28° S latitude, requires only where they affect the further production
10.7 hours of light.30 Of course, the con- of GnRH in a dynamic manner, as well
sequence of this is that species are then as other behavior such as courtship,
limited in selection of breeding sites to nest building, singing, and territorial-
those that have the critical day length. ity. Because these changes occur rather
rapidly following a period of sexual qui-
Hormonal control of reproduction escence, this stage is called the accelera-
tion phase of reproduction.
Stimulus of the ventromedial hypothal- Following a period of gonadal
amus by long photoperiods (i.e., light growth, the ovarian follicles mature
received during the photoinducible and begin to secrete less estrogen and
phase) results in the release of gonad- more progesterone. Progesterone has
otropin-releasing hormone (GnRH) a positive effect on LH secretion and
and prolactin releasing and inhibiting causes plasma LH levels to rise, cul-
factors from neurons in the preoptic or minating in a preovulatory spike that
supraoptic areas of the hypothalamus causes ovulation. The wave of maturing
(fig. 10.12). Only tiny amounts of GnRH follicles causes plasma progesterone
are released and move the short distance levels to rise each day and LH levels to
to the pituitary, where they stimulate the rise as well, each peaking about four to
release of large amounts of the gonado- six hours before ovulation. Birds gen-
tropic hormones, luteinizing hormone erally lay their eggs at the same time
(LH) and follicle-stimulating hormone each day, which reflects the circadian
(FSH), into the general circulation. rhythm of ovulation. However, in some
FSH stimulates the development of the birds, notably domesticated fowl, it takes
gametogenic aspect of the gonads and longer than 24 hours from ovulation
promotes the production of mature ova to oviposition, and consequently, eggs
and sperm. It also promotes the growth are laid later each day, until eventually
of the steroidogenic interstitial tissue of the timing of the LH surge does not
the gonads, but LH is responsible for fall within the sensitive period (4–11
chapter 10

stimulating the synthesis of the steroids hours following the beginning of the
(androgens and estrogens) and their dark cycle, causing the bird to miss an
release into the blood. In the male, the ovulation or skip a day’s egg produc-

306

1stPages_B.indd 306 7/22/20 11:48 AM

 Fig. 10.12. Effects of hormones (boxes) on mammals. In chickens, stimulation of
the brain, gonads, and secondary sex organs the preoptic area of the brain will cause
(right) during early gonadal development (the premature expulsion of an egg via release
acceleration phase of gonadal growth). of posterior pituitary hormones.
The ovulation-oviposition cycle con-
tinues until the clutch is complete. How
Anatomy and Physiology of Reproduction
tion). However, we must remember that this is determined is not fully under-
daily egg production in all birds depends stood. High levels of progesterone may
on the female’s ability to accumulate eventually inhibit ovulation by negative
or mobilize her own resources rapidly feedback on GnRH release from the
enough to produce eggs. hypothalamus. Visual and tactile cues
Expulsion of the egg (oviposition) are also important in the termination of
involves the relaxation of abdominal mus- egg laying, but how birds perceive that
cles and muscular contraction of the shell their clutch is complete remains a mys-
gland, the vagina, and the cloaca. Two tery. During egg laying, levels of prolac-
hormones of the posterior pituitary gland tin (secreted by the anterior pituitary)
induce oviposition in the laying female, rise, and this hormone may also have
oxytocin and arginine vasotocin (avian a negative effect on GnRH release and
ADH). Both hormones cause contrac- thereby suppress further ovulation.
tion of smooth muscle in both birds and Once the clutch is completed, incu-

307

1stPages_B.indd 307 7/22/20 11:49 AM

 bation proceeds. Most females incubate to complete its preparation for winter.
with greater intensity as the clutch In many species the reproductive effort
increases in size, perhaps as a result is terminated by a period of photore-
of increasing levels of prolactin during fractoriness, or insensitivity to long
laying. Brood patch development also photoperiods. This often occurs when
progresses during laying, as rising levels day lengths are still long, perhaps even
of prolactin and of estrogen and proges- before the summer solstice. But the
terone secreted by the ovary promote ecological advantage of such a control
defeathering and vascularization of the is that it allows the young time to grow
ventral abdominal area. In phalaropes, and mature during a period when food
in which the male incubates, testoster- is abundant, and it allows the par-
one and prolactin stimulate the pro- ents time to complete the postnuptial
duction of a brood patch. Contact with molt and to fatten before migrating or
the eggs promotes further increases in overwintering. Through a variety of
plasma prolactin, which in turn pro- experiments with male White-crowned
motes more intense incubation efforts. Sparrows (Zonotrichia leucophrys),
When high levels of prolactin suppress researchers concluded that it is not pos-
the release of gonadotropic hormones, sible to induce any of these latter events
the ovaries regress in size and the without previous exposure to long days;
unovulated, yolky follicles are resorbed. thus, it appears that both reproductive
The role of prolactin in avian and postreproductive events are driven
reproductive behavior beyond this point by the same photoinducible stimulus.31
depends on the species. In birds with In species that breed only once a year,
altricial young, prolactin levels rise individuals that have fledged young
somewhat throughout incubation, peak enter what is called an absolute refrac-
shortly after hatching, and then decline. tory phase, in which they are insensi-
In precocial birds such as the turkey, tive to a long photoperiod. This phase
prolactin levels drop rather sharply is usually short but is followed by a
after hatching, presumably because less relative refractory phase during which
parental care is required in this species. individuals remain sexually inactive,
High levels of prolactin are maintained although they may be responsive to
in adult pigeons and doves for the first long photoperiods (demonstrated
week after the young hatch; in these experimentally). The latter state may
species prolactin stimulates the produc- last for several months, usually through
tion of a special crop secretion, “pigeon’s the winter in temperate species, after
milk,” which is fed to the young. which the cycle is repeated with the
natural increase in photoperiod. Many
Termination of reproduction birds must go through a photorefractory
period to be photostimulated again.
To maximize its fitness, a species We have implied that photorefrac-
should have evolved control mecha- toriness occurs in all birds following
chapter 10

nisms to terminate reproductive activ- fledging of young. In fact, some species

ity when it is no longer energetically can produce several broods in a sea-
feasible to produce young and in time son. These birds start breeding in early

308

1stPages_B.indd 308 7/22/20 11:49 AM

 spring and delay photorefractoriness tory or prewinter fattening, and migra-
until late summer or autumn. In spe- tion (in some). All of these physiological
cies that produce multiple broods, exter- events must be squeezed in between
nal stimuli related to the development fledging young and the first frosts of
of the young or the adequacy of the winter. Most birds must undergo their
environment for rearing young must annual molt at this time simply because
reinitiate the reproductive process. energy demands at other times of the
The gonads do not regress completely year are too high. For example, the high
in these species, and this shortens the costs of thermoregulation in the winter
period between nestings. Pigeons and coupled with diminished food resources
doves continue to produce young as preclude having enough energy to molt
long as climatic conditions allow, irre- then. Costs associated with breeding
spective of photoperiod. This group is and spring migration obviously rule
also known to omit the refractory phase out a complete molt at these times.
in the reproductive cycle. This leaves only the period immediately
There are exceptions to the normal prior to breeding, and some species
pattern of termination of reproduction. do undergo partial body molts at this
If the reproductive effort is prematurely time to acquire their brightly colored
terminated by nest or mate loss early breeding plumage. However, an ener-
in the cycle, many species can renest. gy-demanding complete molt prior
The speed with which renesting occurs to breeding would deplete the energy
depends on a variety of factors, includ- reserve required for spring migra-
ing the stage of the cycle in which the tion and for a successful reproductive
interruption occurred, the physiological season. These constraints leave the
state of the female, and the availability postbreeding period as the best time to
of mates. undergo a complete molt. The advantage
of a postnuptial molt is that the new
Coordination of the Reproductive set of feathers provides residents with
Cycle with Other Events of better insulation for winter and provides
the Annual Cycle migrants with new flight feathers to
Anatomy and Physiology of Reproduction
speed their travel south.
All of the above physiological phe- The cost of the autumn migration is
nomena associated with breeding are a further constraint limiting the repro-
energetically expensive, yet they are ductive period of migrants. Migrants
necessary to produce offspring. For tem- must accumulate extensive fat reserves
perate birds, and especially those that before leaving the breeding site, and
migrate, termination of breeding may this cannot be accomplished until
be explained partly by the demands of both reproductive efforts and molting
the events in the annual cycle that follow are completed. Birds may use various
reproduction. Some optimal balance of environmental cues, such as weather
time and energy must be developed to or food supply, to judge the efficacy of
complete the annual cycle. further reproduction in the face of the
Following the breeding season, birds ­energy-demanding events that follow.
undergo a postnuptial molt, premigra-

309

1stPages_B.indd 309 7/22/20 11:49 AM

 C HA P T E R 11

General Patterns
of Reproductive Behavior

I
n describing the anatomy and phys- ing an attachment between the paired
iology of avian reproduction we birds so that each can be sure that any
focused on the egg and the mecha- young produced are parented by the
nisms needed to produce it and to pair members. Certainty of paternity or
promote its success. Here, we will focus maternity is important, as individuals
on adult birds and their behavior while that put effort into raising offspring that
nesting. Obviously, these topics cannot are not genetically their own will usually
be completely separated, particularly as contribute fewer genes to subsequent
the developmental type of the egg has generations than those individuals that
such a great effect on parental behavior, make an effort to ensure their genetic
so we must keep in mind the interaction contribution. Often, pair formation and
between behavioral responses and the territory acquisition are so closely linked
physiological constraints discussed in that they cannot be separated, while in
chapter 10. other cases one precedes the other. Song
This chapter will confine itself is a large component of the courtship
primarily to the reproductive behavior behavior in many species, but it, too,
of birds showing social monogamy, is quite variable in terms of its role in
the mating system in which one male territory acquisition and mate attraction.
and one female cooperate to raise their To avoid confusion, this chapter begins
offspring. This system is the most com- with a look at spacing mechanisms used
mon in birds, with around 90% of all by monogamous breeding birds; it will
bird species regularly showing monog- then examine the role of bird song in
amous social systems, although recent both the territory and mate acquisition
work on parentage has shown that many processes. The interactions of these will
of these socially monogamous birds are be discussed in a section on courtship
not genetically monogamous. We will and mating rituals, followed by a general
deal with this problem and the other look at nest building and parental care
10% of species with different mating through the reproductive process.
systems in chapter 12.
The first problems for a breeding
monogamous bird are finding a place
to nest, finding a mate, and develop-

310

1stPages_B.indd 310 7/22/20 11:49 AM

 Territories and Spacing ing. Several factors seem to favor this
during Reproduction pattern. First, breeding occurs during
the most productive times of year, which
Chapter 7 suggested that one of the first means that resources are often relatively
decisions a foraging bird must make is abundant and uniformly distributed,
about spacing. Does it forage alone, per- favoring territorial spacing. Also, many
haps defending an area with adequate birds feed their nestlings insects, which
food, or does it feed in a flock of either are more uniformly distributed than
conspecifics or other species? It was fruits and seeds. Both of these factors
suggested that the availability of food tend to produce the relatively abundant,
and a bird’s susceptibility to predation uniformly distributed resources that
were the major factors influencing this favor some system of uniform spacing.
decision. Uniform food distribution As long as these resources occur in hab-
tends to favor spacing behavior, often itats with many suitable nest locations,
territoriality, whereas patchy, irregular such that predators will have a hard time
resources tend to favor flock foraging. finding nests, territorial behavior is fur-
High exposure to predation, as in open ther favored. In fact, the spacing of nests
habitats, tends to favor flocking, while associated with territories may reduce
more protected habitats do not. As you predator pressure by lowering a preda-
may remember, various combinations of tor’s chances of success. Familiarity with
these factors result in a variety of territo- the territory’s escape routes or refuges
rial and flocking patterns in birds. also aids the territory holder in avoiding
Like all birds, breeding birds need predation. Most forested habitats and
to weigh food distribution and predator even most grasslands have thick enough
pressure, but they must also consider vegetation that it is easy for birds to hide
the distribution of acceptable nest sites. their nests during the summer breed-
This factor takes into account both phys- ing season. Such habitats also allow a
ical constraints on nest construction (see greater variety of nest types, which may
below) and exposure of potential nest further reduce predation, as we will see
General Patterns of Reproductive Behavior
sites to predators. The balance of food below in the section on nests and nest
distribution, nest site distribution, and building. A final factor that may favor
predator pressures largely determines territorial spacing is the relative ease
the decision regarding either territorial with which paired territorial birds can
behavior while nesting or some sort of keep other birds out, thus making it
group nesting, generally in what are difficult for other males to mate with the
known as colonies. female of the pair or for other females to
add an egg to the pair’s clutch.
Breeding territories The development of territorial behav-
ior during breeding can be explained
Most monogamous breeding birds using the same model we discussed in
possess territorial spacing during the chapter 7, the economic defensibility
breeding process. Many species that join model of Jerram Brown (1964). In the
flocks during the nonbreeding season case of breeding birds, though, both
show territorial behavior while breed- food and nest site distributions must be

311

1stPages_B.indd 311 7/22/20 11:49 AM

 balanced in the evolution of the appro- many tropical birds with Type B terri-
priate territorial behavior. If nest sites are tories have an area from which they do
widely available, the model deals mainly exclude all conspecifics. While this may
with food dispersion. At the point where be related to resource availability, it may
resources are rich enough that their also be the male’s strategy to ensure that
defense results in greater gains than other males do not copulate with his
the cost of defense, territorial behavior mate.
should evolve (unless constrained by
predator problems). In Type A breeding Nesting in colonies
territories, the defended area includes all
the requirements for the breeding pair to Whereas territorial systems tend to
survive and produce young. As with for- occur when food and nest sites are
aging territories of the same type, these
Fig. 11.1. Distribution of typical multipurpose
territories are generally nonoverlapping
territories in the Blue Tit (Parus caeruleus) in
and vigorously defended by the territory
a forest in the Netherlands. Note the uniform
holders (fig. 11.1).1 Nearly all temper-
size of territories, how little overlap there is,
ate-breeding species show Type A breed- and how the nest boxes provided in this study
ing territories. In contrast, many tropical (green circles are unused boxes, purple circles
forest species with widely dispersed nest are used boxes) are uniformly spaced. In a few
sites show Type B breeding territories, cases a male had two active females within his
for the same reasons suggested earlier. territory (Dhondt, Schillemans, and De Laft
During the breeding season, however, 1982).
chapter 11

312

1stPages_B.indd 312 7/22/20 11:49 AM

 uniformly distributed, colonial nesting Fig. 11.2. A Magnificent Frigatebird (Fregata
tends to occur when food and/​or safe magnificens) nesting colony within a
nest sites are not uniformly distributed. mangrove tree on the island of Barbuda. Photo
Oceanic birds may best illustrate the by John Faaborg.
factors that favor coloniality. Many of
these species can fly long distances each
day searching for prey near the ocean’s islands that are large enough to support
surface. and protect nests but not so large as to
During the nonbreeding season, support many predators. Such protected
they may be fairly uniformly distributed sites are often few and far between, but
across the high seas, but during the the advantages of a safe nesting site
breeding season, since they cannot build seem to outweigh the disadvantages
a nest on the open ocean, they face an of extra travel for these ocean-feeding
irregular distribution of nest sites. One birds. This patchy distribution of safe
option would be to nest along the coast nesting sites leads to coloniality in oce-
General Patterns of Reproductive Behavior
itself, which might allow a long string anic birds (fig. 11.2).
of territories. However, most of these The development of colonial breed-
species travel for many miles in search ing within a species may result in a
of food, so defense of feeding territories giant colony (in some cases millions
would be difficult. In some cases, the of birds) that shares a feeding area and
food supply may be patchy or unpre- a nesting island, but not everything
dictable enough to rule out territorial is shared. Rather, each pair still has a
defense. Thus, a system of territories small nesting territory within the colony
along the coast does not work for these that it occupies and defends from other
species. Additionally, nests along the birds in the colony. This is often termed
coastal mainland may be exposed to a Type C territory. It may be seen as an
nest predators, lessening the chances of extension of the gradient of increasing
success. foraging overlap between pairs and
About the only option left for reduced defended area that we saw in
oceanic birds is to nest on offshore moving from Type A to Type B territo-

313

1stPages_B.indd 313 7/22/20 11:49 AM

 ries. In many species, the size of the when compared to the option of being
territory within the colony is just about widely spaced.
the size of the space occupied by the Breeding colonies are among the
nest and incubating parent. most impressive sights in the bird
Many other birds of the open water world. In some cases, millions of birds
use a similar strategy of colonial nest- may share a single island. While this
ing on small islands. Gulls and terns has advantages, these advantages have
are noteworthy in this regard, as are limits. Food supply may become limit-
many herons and other large coastal ing if colonies get too big. A colony of a
species. When their food supply is fairly million murres may require 200 tons of
uniformly distributed, these colonial food a day. Despite their overall value in
breeders may defend feeding territories predator avoidance, such assemblages
away from the colony. If the food supply cannot help but attract some predators.
is patchy in time or space, flock foraging Thus, when discussing costs and
may be favored. It has been suggested benefits of colonial breeding we must
that in some species the existence of a look both at the general advantages of
breeding colony may be due in part to coloniality and at how these factors may
its value as an information center to aid affect individuals differently depending
colony members in foraging. In these on their location in the colony, their
cases, the breeding colonies also offer feeding habits, and so forth.
some protection against nest predators, Predation on colonial nesters is
so controversy remains over the extent reduced first by the selection of a rela-
to which the exchange of information tively predator-free nesting site when
has favored colonial breeding. possible. Even if predators are present,
Situations may exist where the food colonies offer protection in a variety of
supply of a species is uniformly distrib- ways. In some cases, colony members
uted, but the species is so vulnerable to aid one another by being vigilant, such
nest predation that it requires nesting that it is difficult for a predator to sneak
in a colony for the antipredator benefits up on a colony member without being
of group breeding. We might expect this seen and the colony warned. This idea
in species that are somewhat larger than is identical to the “more eyes” argument
normal, such that they cannot hide their used to favor flock foraging as a predator
nests very well. To date, most colonial defense. In many cases, colonial nesters
breeders seem to be responding to may reduce predation by actively repel-
either limited, predator-free nest sites or ling the predator by mobbing or even
patchily distributed foods, but we would attacking it. If such forms of predator
expect to find varying patterns in the defense do not work perfectly, birds
importance of these factors in selecting nesting near the periphery of the colony
for colonial breeding. will suffer the greatest predation, as they
are the ones a predator will attack before
chapter 11

Costs and benefits of colonial breeding it is seen and repelled. Many studies
have shown that most nest or parent
Breeding as part of a colony presents a losses occur near the edge of colonies,
variety of costs and benefits, particularly and much fighting occurs among the

314

1stPages_B.indd 314 7/22/20 11:49 AM

 birds to obtain a position within the Extensive fighting may occur, offspring
center of the colony. may get lost or even be killed by neigh-
Because age-related dominance boring parents, and diseases or parasites
interactions are part of the territory may be more prevalent. Several studies
acquisition process within colonies, it have recently shown rather important
is not surprising that young birds nest effects from the latter, including the
near the edge of colonies, with older possible cessation of breeding among
birds in the middle. colonial seabirds in Peru when tick pop-
Even if predation losses occur within ulations get too large. In other examples,
the colony with a certain regularity, there colony sites have been deserted when
are ways for colonial birds to reduce parasite numbers reach high levels.
losses. One of these has been termed the Monogamous colonial male birds
Fraser Darling effect, after the person face a problem with confidence in pater-
who suggested it.2 This idea is that colo- nity. With so many other males around,
nial nesters can effectively swamp their a male must be concerned about ensur-
predators, thereby minimizing losses, by ing that his mate copulates only with
synchronizing their breeding activities him. While in nearly all monogamous
such that eggs and young are available birds the male is particularly attentive to
to predators for the shortest period. If his mate during the most critical fertile
we assume a set number of predators period around egg laying, in colonial
that eat a certain number of prey items birds this attentiveness is carried to
each day, we can see how a colony that an extreme. During the critical period
synchronized its nesting would suf- the female usually cannot do anything
fer much smaller losses than one that without her male around her, defending
nested over longer periods. This effect her from other males. Of course, once
has been shown in several studies, along a male has ensured the paternity of his
with the associated observation that both mate’s offspring and the clutch is laid,
early and late breeders in a colony suffer he may also attempt to mate with other
greater predation losses. females that are still laying.
General Patterns of Reproductive Behavior
The foraging advantages of colonial The above facts suggest that most
breeding have already been discussed. species should be either territorial or
These advantages may be limited when colonial, which is generally the case.
the colony becomes so large that greater Some species, however, have individu-
distances must be traveled to find food, als that show both patterns, and there
even if these travels are aided by infor- are cases in which nests are fairly well
mation relayed within the colony. There spaced, suggesting territoriality, yet
is some evidence that growth rates and when considered in a larger spatial
fledging weights of some young seabirds context these territories are clumped,
differ depending on colony size, pre- suggesting a loose form of coloniality. As
sumably because large colonies deplete with so many other ecological patterns,
the food supply around them. some species are exceedingly flexible in
The other disadvantages of nesting responding to resource variation.
in colonies are the result of simply hav-
ing so many animals so close together.

315

1stPages_B.indd 315 7/22/20 11:49 AM

 Bird Song and Reproduction the territory. Should a male do this,
song is one of the first ways that two
One cannot think of spring and the males may start to assess one another’s
breeding season without thinking of dominance status. While such assess-
birdsong. It is one of the most obvi- ment often includes other displays and
ous characteristics of this period, even threats, song is often the first cue used
though not all birds sing. We have by competing males. Such ritualized
already discussed some of the forms of behavior as song and threat replaces
avian vocal communication; here we actual physical combat in most cases,
focus on those vocalizations generally which is generally advantageous to both
known as song, which are distinctive males.
because they are so closely related to Although people have observed
reproductive behavior and generally the role of song in territory acquisition
occur most frequently during reproduc- and maintenance for decades, some
tion. Birdsong also usually occurs only recent experiments with Great Tits
in males, which contrasts with those (Parus major) have reinforced our ideas
vocalizations usually classed as calls, about the role of song in this regard.3
which may occur in either sex through- All the territorial males of a study site
out the year. Because the distinction in England were removed after they had
between songs and calls is sometimes established territories. In part of this
unclear, some have defined song as the habitat, loudspeakers played tit calls
most complex vocalizations given by the regularly; in a second part, a control
male. noise was played; in the rest, no play-
back occurred. Reoccupation of the
Functions of birdsong “empty” territories occurred much more
slowly in the territories with playback of
Birdsong serves a variety of functions tape-recorded calls, presumably because
on many different levels, not all of them of the repelling effect of birdsong to
important to each species. Although nonterritorial birds. It should be pointed
lists of several dozen functions have out, however, that intrusions occur even
been made, birdsong appears to be most with song, suggesting that birdsong
important for (1) territorial behavior, (2) minimizes conflict for territories, but
mate acquisition, (3) synchronization of that it must occasionally be backed up
reproductive processes, and (4) individ- by threat and other aggressive behavior.
ual recognition. Let us examine each of Mate acquisition. Songs appear to be an
these functions in turn. important means by which males attract
Territorial behavior. Males use songs in a mates to themselves or their territories,
variety of ways to acquire and maintain although it is often difficult to separate
territories for breeding. When a male the relative importance of these two
arrives at a location he chooses for a factors in female choice. A typical song
chapter 11

territory, he generally starts to sing. This advertises that a male has a territory
song may serve to advertise his occu- and/​or is willing to mate. As we will
pancy of the site, which may discourage see, the call may also provide the female
other males from attempting to invade with information on the status of the

316

1stPages_B.indd 316 7/22/20 11:49 AM

 particular male. In species that use calls Individual recognition. Recent work
to attract mates but not to advertise a has shown that birdsong is an effective
territory, song often stops after mating mechanism for individual recognition.
rather than continuing at some level Such recognition may be important in
throughout the breeding process. Some male-male interactions such as territo-
species have a song for mate attrac- rial defense (see below), male-female
tion and a separate song for territorial interactions on the territory, and par-
defense, with the frequency of these ent-offspring interactions.
songs changing as a male goes from ter- All of the above functions do not
ritory establishment to mate attraction accompany the song of each species.
early in the spring. Rather, great variation occurs in the role
An important part of attracting a of song both within and among species.
mate is, of course, attracting a mate of With such variation, it is not surpris-
the proper species. Thus, song serves as ing that many types of songs occur. In
communication both within and among addition to potentially unlimited vari-
species. A species’ song is an import- ability, birdsong also has the advantage
ant way of maintaining reproductive over other forms of communication of
isolation so that an individual does not requiring little energy, vanishing quickly
breed with a mate of another species, once the call is made (thus making it
thereby producing hybrid offspring with hard for predators to find the singer),
low chances of success (see chapter 4). and covering large distances. With
Thus, while natural selection may favor such apparent ease of communication,
variation within the song of a species, unlimited song types could conceivably
so that information about the charac- occur. Since they do not, we need to look
teristics of individual males might be at some of the constraints on birdsong.
communicated, this variation must not
be so extreme that all members of the Variation in birdsong
species cannot recognize it as the song
of conspecifics. Birdsong varies among species, presum-
General Patterns of Reproductive Behavior
Synchronization of reproductive pro- ably to help ensure reproductive isolation,
cesses. Once a pair-bond has formed, and within species on regional, local, and
there is evidence that birdsong serves individual scales. Yet some species show
as an important stimulus to help coor- virtually no variation in song over vast
dinate the behavior of the birds through geographical distributions.
the various physiological stages needed To understand the interspecific dif-
for successful reproduction. Experi- ferences in song, we must consider both
ments with various species have shown the purposes of the song in each species
that females exposed to singing males and the constraints within which these
build their nests faster or better, lay eggs songs are produced. Most important
earlier, and develop stronger incubation among these latter factors may be what
behavior than females isolated from is called the acoustic environment, the
male song. Male song may be important way that sound waves travel in different
in maintaining the pair-bond through- habitats.
out the reproductive process. Studies have shown that sound

317

1stPages_B.indd 317 7/22/20 11:49 AM

 waves of different frequency attenuate surveys of birdsong suggest that this
(lose energy) differently based on both is true by showing differences in the
habitat type and elevation within a dominant frequencies of songs used in
habitat type. For example, low-frequency different habitats (fig. 11.3).4 Although
sound waves travel better in forest this might favor convergence in song
habitats than high-frequency sounds but type among co-occurring species, the
dissipate rapidly in open habitats. Sound requirements of reproductive isolation
attenuates more rapidly in deciduous favor species with different songs. Most
forest than in coniferous forest. songs probably represent a compromise
These studies suggest that birds among these factors, with song develop-
living in particular habitats should ment favoring the best frequencies for
adopt songs that travel best within these long-term communication while varying
habitats to achieve the most efficient such parameters as song length, timing,
long-distance communication. Several and structure.

Fig. 11.3. Distribution

of the frequencies
dominant in the songs
of Panamanian birds
in different habitats,
with rainforest on the
bottom, edge habitat
in the middle, and
grassland habitat on
top (Morton 1970).
chapter 11

318

1stPages_B.indd 318 7/22/20 11:49 AM

 If the need for species recognition is lack of variation seems to be related to
important in the evolution of song diver- the absence of any role of learning in the
sity, we might expect that species living development of vocalizations. If a young
in more diverse communities would rooster or pigeon is raised in isolation
show more complex song types, as these so that it can hear no other bird sounds,
would be necessary for the proper recog- or even deafened so that it can hear
nition of the large number of coexisting nothing, it still sings almost perfectly. In
species. We might also expect that each these species, song seems to be almost
species in a diverse community might entirely a genetic trait that is fixed
show somewhat less variability in song throughout the population in much the
type, since the possibility of mistakes in way that plumage and size are. Despite
species recognition might be higher in this reduced variation in song character-
such communities. While there is some istics, many of these species use songs
evidence that birds living in complex for the full variety of functions men-
communities have more complex songs tioned above.
and those in simple communities have Species with songs that show
more variable songs, the great number significant variation both within and
of intraspecific factors that affect song among populations are found primarily
variation may mask any patterns based in the oscine suborder of the Passeri-
on the role of interspecific factors in formes and the parrots (Psittaciformes).
song variation. In the same manner, Until recently, these two groups were
these interspecific constraints may limit thought to be distantly related, but recent
variation favored by intraspecific consid- genomic work has suggested that they
erations. may be closely related. These groups
Variation in songs within species is are also distinctive because it appears
generally approached on either a local that all have an element of learning in
or regional basis. Regional variations the development leading to adult song.
are often termed dialects, as they resem- The degree of variation either within or
ble in many ways the regional varia- among populations seems, then, to be
General Patterns of Reproductive Behavior
tions found within human languages. a function of how this learning is done,
Although often approached separately, when it occurs during development, how
both types of variation are related to young males disperse, and how accu-
song function, inheritance, social behav- rately learned songs can be reproduced.
ior, and learning mechanism. Before we examine the learning pro-
Many species show virtually no cess, let us look at some general patterns
regional variation and little individual of song variation and their apparent
variation in vocalizations. Among these functions.
are most of the nonpasserines (doves, Small amounts of individual vari-
chickens, cuckoos, and such) plus the ation seem to be related to individual
more primitive suboscine passerines recognition. It has been shown that even
(flycatchers, antbirds, woodcreepers, species with quite simple, low-variability
and ovenbirds). It has been said that songs have enough information within
these groups do not sing, although this each song that individual birds can tell
depends on the definition of song. This one another apart. Such recognition is

319

1stPages_B.indd 319 7/22/20 11:49 AM

 advantageous in reducing the time and territory” but are pointing out that “I am
energy spent in male-male conflicts, for a male with a complex song that shows I
if a male knows the identity of a singing have a lot of experience, high dominance
male, he can remember his status rela- rank, and a territory.”
tive to it and act accordingly. Such proclamations of sexual status
The classic studies of this sort of can affect interactions with both males
interaction have been done with White- and females. In nearly all studies to
throated Sparrows (Zonotrichia albicollis) date, it appears that songs with greater
on their breeding grounds.5 Males of variability are those that are associated
this species sing rather simple songs with (or give the singer) higher status.
that do not vary greatly. These are used In the experiments with the Great Tit
at least in part to repel rival males discussed earlier, subsequent repe-
from territories. Once a set of males titions showed that territories with
has established territorial boundaries, loudspeakers that played rather diverse
aggressive interactions are minimized repertoires of songs excluded intruders
by the recognition of the song and longer than territories where simple
location of each neighboring male and songs were played. Males are apparently
the failure to respond to neighboring more intimidated by complex songs. It
songs from a known bird in the proper has been suggested that this is because
location. The same experiments have complex songs are learned, such that the
shown, however, that playing the song of singer of complex songs is most likely
an unknown bird will cause an imme- also an older, more dominant bird. It
diate response among territorial birds, has also been suggested that such songs
as will the playing of a taped call of a tend to confuse potential intruders into
known bird from an improper location. thinking that several males live on a
In both these cases, the territorial male territory, rather than just one, although
recognizes a serious threat to his terri- this idea has little support.
tory and responds in the proper manner. Females also seem to respond to
In general, when song variation is more complex songs, possibly because
used only to identify individual males of the age-related factor mentioned
within a group of males, the amount of above. Larger song repertoires have been
variation should be small. Some spe- shown to attract females more rapidly
cies, such as the Northern Mockingbird than smaller repertoires and stimulate
(Mimus polyglottos), show large varia- stronger nest-building activities (fig.
tions in song traits among individuals, 11.4).6 Certainly, if males with complex
much larger than would be necessary for songs can acquire territories better than
individual recognition alone. In these males with simple songs, it is advanta-
cases, it appears that the individuality of geous for females to choose males with
the song has gone past mere recognition complex songs. In this way, song reper-
to a statement about status that the male toire may serve much the same function
chapter 11

is proclaiming to both other males and as plumage characteristics, size differ-

potential female mates. In some ways, ences, or other behavior in determining
males using these more complex songs the winners of competition for mates
are not just saying “I am a male with a and territories. All can be considered

320

1stPages_B.indd 320 7/22/20 11:49 AM

 Fig. 11.4. Number of
nest strings gathered
by female canaries
exposed to either
large (top) or small
song repertoires
(Kroodsma 1982).

secondary sexual characteristics subject male interactions may favor smaller vari-
General Patterns of Reproductive Behavior
to sexual selection. This idea is rein- ation in song types. The roles of song
forced by the fact that in several species in the breeding process may also affect
that are polygynous (i.e., males can mate singing patterns; males that sing only to
with more than one female at a time; attract females may cease singing after
see chapter 12), males have much larger they are successfully paired, while those
song repertoires than are found in their that use song to repel males will con-
monogamous relatives. tinue. The typical traits of songs associ-
The role of song variation in both ated with these two functions, and how
repelling males and attracting females they sometimes conflict, are summa-
sometimes results in conflicting natural rized in table 11.1. As with many other
selection pressures on song types. While traits, most species strike some balance
females may prefer males with large between songs being specific enough for
song repertoires, males may not respond species recognition and variable enough
as strongly to those parts of the song to satisfy the other natural selection
with which they are unfamiliar, so male- pressures.

321

1stPages_B.indd 321 7/22/20 11:50 AM

 Table 11.1.
Some diagnostic characteristics of the two main types of song in male passerine birds
main proxi- female attractions male repulsion
mate function (e.g., sedge warbler). (e.g., great tit).
Song structure Large syllable repertoire. Small syllable repertoire.
Variable sequencing. Stereotyped sequencing.
Songs not repeated. Song types repeated.
Continuous singers. Discontinuous singers.
Contextual Sings in territory before pairing Sings in territory after pairing.
correlations and stops after. Sings in response to playback after
Does not sing in response to play- pairing.
back after pairing. More likely to be resident.
More likely to be migratory.
Direct effects on No matched countersinging oc- Matched countersinging occurs.
males curs. Speaker replacement experiments
Speaker replacement experiments repel ­rival males and are more effec-
have no significant effect. tive with larger repertoires.
Direct effects on Males with larger syllable reper- Males with larger song type reper-
females toires do not obtain better territo- toires obtain ­better territories.
ries.
Males with larger syllable reper- Males with larger song type reper-
toires attract females first. toires do not attract females first.
Main selection Intersexual selection. Intrasexual selection.
pressure involved
Source: Catchpole 1982.

Because variable songs involve bird song in these species, it also shows
at least some aspect of learning, and how important the aggressive inter-
because it is likely that particular actions associated with singing are in
phrases (termed syllables) have no reinforcing the function of song.
specific function other than enlarging The occurrence of dialects varies
the song repertoire, it is not surprising greatly among species, as do the bound-
that songs vary geographically, giving aries between dialects. In some cases,
us the dialects mentioned earlier (fig. rather sharp boundaries occur between
11.5).7 Studies with recorded playbacks dialect types, such that reinforcement of
have shown that many species will not these boundaries by natural selection is
chapter 11

respond to all or to parts of songs used implied; in other cases, dialects seem to
by that same species in a different area. change gradually with distance. Perhaps
While this observation reinforces the the classic study on the distribution of
role of learning in the development of dialects was done on the Rufous-collared

322

1stPages_B.indd 322 7/22/20 11:50 AM

 Fig. 11.5. Sonograms that show graphically
the song of the Bewick’s Wren (Thryomanes
bewickii) in four different locations (Kroodsma
1985).

1stPages_B.indd 323 7/22/20 11:50 AM

 Sparrow (Zonotrichia capensis) in Argen- explanations suggest that dialects serve
tina.8 Researchers recorded calls along as a mechanism for what is called
an altitudinal gradient from grassland assortative mating. (Assortative mating
through montane forest habitats and occurs when an individual bird chooses
found that dialect boundaries coincided its mate from a certain subset of the
with habitat changes, such that several population rather than at random; in
dialects were found as one proceeded up this case, females would select males
a mountain, but that these dialects might by dialect.) A female might be selec-
not change for great distances at the tively favored when mating with a male
same elevation through the mountain singing the dialect that her father sang
range (fig. 11.6). Studies of the White- because that male would supposedly
crowned Sparrow (Zonotrichia leucophrys) be better adapted to the environment
in San Francisco Bay have shown some- from which the female came than a
what similar patterns, although studies male singing a different dialect. In other
of this species elsewhere have found words, the dialect may reflect small
more gradual boundaries. morphological or behavioral adaptations
A variety of explanations for the to a particular microhabitat and thereby
adaptiveness of dialects have been
proposed. The fact that Rufous-collared
Fig. 11.6. Changes in the trill interval of songs
Sparrow dialects coincided with habi-
of the Rufous-collared Sparrow (Zonotrichia
tat changes suggests that the dialects capensis) with changes in altitude in South
reflected changes in the acoustic envi- America (Nottebohm 1975). Smaller variation
ronment with resultant differences in in trill intervals within similar altitudes may
the selective pressures on the optimal be related to vegetation changes within these
characteristics of the song. Most other altitudes.
chapter 11

324

1stPages_B.indd 324 7/22/20 11:50 AM

 serve as a signal allowing a bird to mate affect communication in any meaningful
with birds most like itself, thus pro- way. This controversy as to whether song
ducing young presumably well adapted dialects are adaptive or simply learned
to that habitat. This sort of inbreeding social traits remains to be resolved by the
can be good in areas where habitats are large amount of research presently being
rather variable, as long as populations done in this area.
are large enough that too much inbreed-
ing does not occur. Males might choose Learning of birdsong
to remain within the zone where their
dialect is sung for the same reasons. As researchers have worked to under-
Alternatively, it has been suggested stand why birds sing the types of songs
that dialects are used to promote assor- they do, they have discovered how
tative mating where a female decides important learning is in determining
against mating with a male that sounds birdsong variability. With this realiza-
like her father. This would be because tion, the questions they ask have often
mating with a male of a different dialect changed from why birds sing to how
would promote outbreeding and pro- they learn to sing, with the hope that
vide greater genetic diversity. In this answers to that question might provide
case, males might move to areas where insight into the earlier questions on the
different dialects occur to increase their function of song. Studies of the learning
chances of mating. of birdsong have provided tremendously
These opposing ideas about the role significant information on the basic
of dialects may both be correct, given the learning process, much of which has
many variables involved in mate choice proved important to our understanding
in different species. Whether inbreeding of learning in all animals, including
or outbreeding is of selective advantage humans.
would depend on the balance among a Much of the work on learning mech-
variety of ecological and genetic factors. anisms in birds has involved experi-
There is evidence in some species that ments in which young birds were raised
General Patterns of Reproductive Behavior
males always disperse in the direction in acoustic isolation and then exposed
of the center of the distribution of their to different auditory cues at different
dialect, while other species seem to move points in their development. One of
randomly with respect to dialects. In a the earliest studies still illustrates this
few species, dialects are not learned until technique well. William Thorpe studied
the male is nearly a year old, at which the Chaffinch (Fringilla coelebs), a com-
time he learns the local dialect. This mon European finch with a distinctive
certainly does not promote inbreeding. song.9 He found that if a single male
Other workers have suggested that was raised in total isolation, it could sing
many, if not all, dialects may not be only a simple song when it became an
adaptive at all. These scientists think that adult. Yet if a single male was caught
song dialects are analogous to regional in the fall, when it was several months
dialects in humans; they reflect charac- old, and then kept in isolation, by the
teristics learned during development that next spring it could sing a song that was
vary among areas but that really do not very nearly normal. Thorpe found that

325

1stPages_B.indd 325 7/22/20 11:50 AM

 putting several young in isolation from auditory template, learning phase
birth resulted in songs that were much (including sensitive period), and motor
more complex than those sung by a sin- phase (practice)—are still the chief focus
gle individual. These songs were shared of studies on birdsong.
by the group of birds but were unlike the Work with a variety of species has
wild type song. A group of males caught resulted in the recognition of four types
in the fall and then kept together sang of sensitive periods. In some species the
normal songs the next spring. After one sensitive period occurs during just a few
year of age, the songs of these birds did weeks in early life, perhaps as a nestling
not change. or fledgling. Studies with the White-
This pioneering experiment sug- crowned Sparrow suggest that a 10- to
gested several characteristics of birdsong 50-day sensitive period exists among
learning that are still being studied today. birds raised in isolation. At this time,
First, it is obvious that there is a period young birds presumably learn songs
when a young bird learns by listening; from their fathers or nearby males that
at this time it is critical that he be able live within similar habitats.
to hear another male sing. Not sur- In other species, the critical period
prisingly, scientists call this the critical seems to occur during the spring when
period. In the Chaffinch it occurs early the males are nearly one year of age. At
in life, as birds exposed to songs during this time they listen to other males of
the summer could sing nearly normal their species and, with practice, develop
songs if captured and isolated in the a song like that of these other males.
autumn. After one year of age, no learn- Once this is accomplished, however, the
ing seemed to be occurring. Second, the song is fixed throughout life. In some
study showed that social interactions other species, sensitive periods seem to
affected learning, as the small groups occur several times during the first year
of males were able to learn songs better or year and a half of life, after which
than isolated individuals. Some of this the song becomes fixed. Finally, a few
effect seemed to result from the stimu- species seem to have no sensitive period
lation offered by other birds, and some as such but are able to add to their song
may have resulted from practice. Later repertoire throughout their lives.
experiments with deafened birds showed In addition to variation among
that when birds could not hear other species in aspects of the sensitive
songs, normal singing behavior could period, studies have shown that varia-
not develop. Finally, Thorpe’s results sug- tion in sensitive period occurs because
gest that all young birds have a geneti- of changes in photoperiod or hormonal
cally determined, simple song that they levels. Social interactions may also be
will sing if they do not have the chance to important in determining sensitive
learn more complex variations, but they period. Some recent work also suggests
will modify it greatly if given the chance. that some of the techniques of earlier
chapter 11

This internal pattern of song is often studies may have given misleading
termed the auditory template, as it is the results because of the extreme sensitiv-
underlying program on which learning ity of young birds. For example, studies
will operate. These three ­attributes— with tape-recorded calls suggest a 10- to

326

1stPages_B.indd 326 7/22/20 11:50 AM

 50-day sensitive period for White- and human learning have made studies
crowned Sparrows, but studies using of the former extremely exciting.
exposure to live adults have extended
this period to at least 60 days. Special cases of birdsong
The auditory template not only pro-
vides a basic song that can be sung in Even though our brief look at the char-
the absence of any learning, but it also acteristics of birdsong has stressed the
seems to serve as a filter for the learning amount of variation that occurs, a few
process. In the most extreme case, a bird even more extreme cases of birdsong
in the sensitive period simply does not must be discussed. Although these tend
respond to certain sounds, such that one to conform to the functions of song
cannot teach the species certain songs. suggested above, they represent unusual
Yet this individual may be very sensitive mechanisms for accomplishing these
to other song types, particularly those functions.
similar to the ones sung by males of that In most species, only the male
species. Playback studies have shown possesses what we think of as song and
that certain phrases may be learned what ethologists call primary song. Yet
with as few as a dozen exposures, in many species, females are known to
while others will be learned only after sing songs, and while many of these are
repeated playing and in the absence of somewhat simpler songs known as sec-
the species’ normal songs. In addition ondary songs or subsongs, a few females
to the variability in sensitivity within sing primary songs. The functions of
this template, there is great variation in female song probably parallel those of
accuracy among species, such that some male song, as it may help to maintain
species may sing more variable songs pair-bonding and repel territorial intrud-
simply because they seem less willing or ers. There is some evidence, particularly
able to copy exactly the sounds to which from tropical species that maintain year-
they are exposed. round territories and pair-bonds, that
A great deal of research is still being female song is directed at other females
General Patterns of Reproductive Behavior
done on learning in birds, both because in an attempt to repel any intruding
of its intrinsic interest and because female.
of its possible applications for under- Most female song does not occur
standing human learning and neural apart from male song; rather, male and
physiology. Recent work has shown that female may sing together in what is
the maintenance of sensitivity to song known as duetting. In some species,
throughout life seems to require the duetting involves simply the synchroni-
continued growth of nerve cells, at least zation of fairly typical male songs with
in canaries. If the neural mechanisms a female response, but in other species
responsible for this growth of brain cells the male-female interaction has devel-
can be identified, perhaps we can come oped such that a typical species-specific
up with a means of stimulating growth song is composed of phrases contrib-
of human brain cells later in life. Even uted by both sexes. So far, 222 species
if this does not lead to a cure of disease, in over 40 families have been shown to
similarities between birdsong learning duet. Among these are about a third of

327

1stPages_B.indd 327 7/22/20 11:50 AM

 the wrens (Troglodytidae) and shrikes still argue about the ultimate cause of
(Laniidae), and both passerines and this loss. Some suggest that large song
nonpasserines. There are more tropical collections are good for intimidating
duetting species than temperate species; neighboring males, while others sug-
for example, there are over 100 duetters gest that they are good only for attract-
in Panama compared to only 23 in North ing females. Several of the New World
America, despite similar total species mimics (of the family Mimidae) live in
lists for these regions. This geographic edge habitats, where their imitations
distribution may be explained by most of the songs of neighboring residents
duetters being territorial throughout the are often accompanied with aggressive
year and usually maintaining a continu- behavior directed at these residents.
ous pair-bond. This suggests an aggressive, territorial
Evidence suggests that these duets function for mimicry, but other studies
serve the same variety of functions that have shown that females select males
normal male song does, with as much with the most diverse songs, irrespec-
variation among species. Duetting tive of territorial characteristics. These
seems to be advantageous in reinforc- songs may be an attempt by a male to
ing pair-bonds, and perhaps in keeping manipulate neighboring birds and a
track of mates while foraging in thick way to impress a female; as a result,
tropical vegetation. The detailed learn- the vocal attributes of mimics can be
ing involved in many duets between impressive. Although the Northern
pair members may serve to announce Mockingbird is perhaps the best-known
to potential intruders both the existence New World mimic, the champion singer
and intricacy of the pair-bond between (in terms of variety) may be the Brown
the territory holders. Thrasher (Toxostoma rufum), which has
Earlier, we mentioned that large been known to sing over 2,000 differ-
song repertoires are often favored as a ent songs, in contrast to fewer than 250
sign of dominance or experience, but in the mockingbird.10 The Australian
that these complex songs are apparently Superb Lyrebird (Menura novaehol-
limited by selection favoring simpler landiae) not only mimics other species
songs for specific identification. When with which it coexists but can mimic
complex songs occur in a species, there other environmental noises, including
also appears to be a long, if not lifelong, cameras, car alarms, and chain saws
sensitive period that allows the learn- (and has a well-known YouTube film).
ing of new phrases in the song. In a Although it is still arguable whether
few species, the factors limiting large mimicry is an attempt by one species
repertoires seem to have broken down, to manipulate the behavior of several
and incredibly complex songs occur. others through song, there are cases
To develop such songs, these singers where one species does interact with
often repeat many (if not all) the sounds another species through convergence
chapter 11

they hear in their environment in what in song structure. This often occurs in
is known as mimicry. While mimicry those species that are interspecifically
seems to be the result of the loss of con- territorial such that males of one species
straints on song complexity, scientists acquire and defend territories from both

328

1stPages_B.indd 328 7/22/20 11:50 AM

 conspecific and heterospecific males produce on hollow trees. These nonvocal
(see chapter 7). To achieve efficiency in sounds have added greatly to the variety
this endeavor, the species have nearly of sounds available for communication
identical songs that seem to function in birds possessing only limited abilities
among species much as they would to produce vocal song.
within species. Although the occurrence
of interspecific territoriality has been Courtship and Mating Behavior
questioned, several recent studies have
shown this sort of spacing behavior Successful mating with a female and the
and the convergence in song types that production of offspring are the ultimate
often accompanies it. Even though this purposes behind whatever territorial and
has been documented, many questions singing behavior the male of a species
remain about the evolution of such displays. In monogamous species, this
a system and some of the behavioral involves the formation of a pair-bond
details that accompany it. For example, between the male and the female. This
the Philadelphia Vireo (Vireo philadel- pair-bond reduces aggressive tenden-
phicus) and the Red-eyed Vireo (Vireo cies between individuals and increases
olivaceus) are known to be interspecifi- sexual interaction. In most temperate
cally territorial over parts of their range species, pair-bonds are formed for a sin-
in Canada11 and they sing nearly identi- gle breeding season, but in many geese,
cal songs, even though they do not look swans, and tropical birds, these bonds
alike. The role of aggressive behavior seem to last for life. The House Wren
in addition to singing in establishing (Troglodytes aedon) is unusual in that
territories among species needs further most pairs break up after each success-
examination. ful nesting attempt, such that an individ-
ual may have two or three mates during
Nonvocal sounds a single breeding season.
In nearly all cases, final bonding is
Birds make some sounds that are not accomplished through ritualized behav-
General Patterns of Reproductive Behavior
produced by the syrinx but serve the ior known as courtship displays. These
same functions as song. These nonvocal displays may or may not be associated
sounds can be manufactured in a variety with either singing by the male or the
of ways. Many of them are mechanical acquisition of a territory. Some migra-
noises made by the feathers, usually tory species form pair-bonds before
by the movement of air through the arriving at the final breeding territory,
feathers. In some cases, such as the while in others, the territory is first
courtship dives of Common Nighthawks occupied by the male and becomes
(Chordeiles minor), the manufacture of part of what he offers a female in the
noise requires no feather modification, formation of the pair-bond. Most tem-
but some species have feathers that perate-breeding ducks mate on their
are modified to aid in the production wintering grounds and migrate together,
of sound. Other birds make sounds by sometimes thousands of miles, to the
interacting with their environment, such breeding territories. Among temperate
as the drumming noises woodpeckers forest birds, many pairs break up after

329

1stPages_B.indd 329 7/22/20 11:50 AM

 breeding, but the tendency for both male displays can be categorized into four
and female to return to the same breed- groups: (1) song (which we have already
ing territory results in the same pairs discussed); (2) display dances, flights, or
forming in successive years. Lifelong postures; (3) courtship feeding or related
pair bonds occur among tropical species activities; and (4) courtship nest build-
with territorial or flocking behavior that ing. Many of these appear to have their
favors continual interaction between roots in normal maintenance behavior
members of the pair. that has become ritualized in a way that
Although it is difficult to generalize now gives them sexual connotations.
about such a variable trait as courtship For example, courtship feeding and
display, it does appear that species that ritualized nest building are obviously
possess complex songs and pronounced derived from functional behavior found
territories often have rather simple later in the nesting cycle, and many
courtship displays, whereas species with other displays are derived from aggres-
small territories and simple or no songs sive behavior. In all cases, behavior has
often have more elaborate courtship evolved a special meaning through time
displays. It may be that pronounced to serve as a signal between male and
territoriality and song serve in part as female about such matters as readiness
the displays that initiate pair formation and willingness to mate.
and maintain it throughout the nesting Courtship displays of males or
cycle. When territories are small and/​ females can be classified as postures (if
or songs are absent, displays seem to they are generally stationary), parades
serve the function of pair-bonding. In or dances (if they move on the ground),
colonial birds, these displays may con- or flights (if they occur in the air). These
tinue throughout the nesting cycle as a categories are not totally exclusive, as
device to ensure individual recognition all incorporate some degree of postur-
between the paired birds. ing either with or without movement.
Courtship displays serve a variety of Some of the most unusual postures are
functions in addition to pair-bonding. those found in seabirds, where both pair
There is evidence that these displays members participate in displays, usually
between pair members tend to synchro- at the nest site. Perhaps because of the
nize the birds’ levels of sexual readiness, limited space available to colonial nest-
eventually resulting in ovulation by the ers and because the crowded skies make
female, copulation, and fertilization. The dancing or flight displays difficult, these
percentage of successful copulations birds have evolved intricate postures that
appears to increase with the time a pair serve the display and recognition func-
has to display before egg laying. The tions (fig. 11.7). Often, these continue
cues from these displays are also criti- throughout the breeding cycle.
cal in stimulating the whole hormonal Parades or dances require more
cycle that accompanies breeding. Finally, space and thus cannot occur on the
chapter 11

courtship displays are a way that species small territories of colonial birds. Such
ensure that they do not breed with a colonial nesters as Western Grebes
different species. (Aechmophorus occidentalis) display away
The great variety of courtship from the nesting site, using elaborate

330

1stPages_B.indd 330 7/22/20 11:50 AM

 Fig. 11.7. Unusual courtship postures
or behaviors in the Blue-footed Booby
(Sula nebouxii), Western Grebe
(Aechmophorus occidentalis),
Magnificent Frigatebird (Fregata
magnificens), and Great Crested
Grebe (Podiceps cristatus).

1stPages_B.indd 331 7/22/20 11:51 AM

 synchronized head movements followed
by a “walking on water” sequence. In
many species of cranes, display dances
are done on the wintering grounds or
during migration when large groups of
males display together to attract mates.
Display flights are commonest among
open-country birds and birds of prey.
These may include only the male or
both the male and female. Hawks and
hummingbirds are renowned for their
spectacular aerial displays (fig. 11.8),12
while larks and pipits often combine
aerial flights and song for their displays.
Courtship feeding is a common
courtship display. In most cases,
the male provides a food item to the
female, usually with an accompanying
display. Sometimes such feeding is an
important supplement to the diet of the
female throughout the nesting process,
although in other species it is just a
ritualized display that occurs early in
the pair-bonding process. This behavior
seems to have evolved from the begging
behavior of nestlings and fledglings,
as many females adopt similar beg-
ging postures before courtship feeding
occurs. Such behavior may also be adap-
tive as a way for the female to evaluate
the relative ability of the male and his
territory to provide food for her and her
offspring.
In a few species, courtship feeding
seems to have become ritualized to
the point that no food is involved but
behavior that was formerly related to
feeding has become a display. While
some seabirds display courtship feeding,

Fig. 11.8. Sketch showing the various phases

of the aerial display of Anna’s Hummingbird
(Calypte anna) (Stiles 1982).

332

1stPages_B.indd 332 7/22/20 11:52 AM

 where the male brings a fish to his mate, however, by the fact that most monoga-
albatrosses and some other seabirds mous males assist in nest-related behav-
engage in bill sparring as a courtship iors after courtship, which tends to favor
and pairing ritual, presumably in place more cryptic coloration. As we will see
of exchanging food. in chapter 12, in species in which males
Another reproductive behavior that serve only to inseminate the female and
seems to have taken on a courtship func- in which they have the potential to mate
tion is that of nest building. In many with many females, sexual dimorphism
species, males will build nests and show may face virtually no selective limits on
them to prospective mates as part of the extremeness of plumage, size, or
the courtship ritual (fig. 11.7). In some behavior.
species, several nests are constructed, The degree of dimorphism in a
and the female may use the number of monogamous species is often related to
nests as a cue to the status of the male. the type and intensity of displays. When
In many species, this display nest is two individuals of a monomorphic spe-
only that, and the female builds the final cies meet, they must first communicate
version that is used for reproduction. which sex they are before they proceed
Inasmuch as all of the above dis- with further courtship displays. Quite
plays and their accompanying mor- obviously, if two males meet, the reac-
phological adaptations are involved in tion will be different than if a male and
determining the success of an individual female meet. With dimorphic species,
at reproduction, they can be consid- individuals can immediately recognize
ered secondary sexual characteristics. the sex of another individual, so they can
These may be related to interactions proceed accordingly with appropriate
both between the sexes and among courtship behavior. In these dimorphic
members of the same sex. The relative species, displays often accentuate the
importance of interactions between the secondary sexual characteristics distinc-
sexes and within sexes, along with the tive to the species. For example, bright
relative roles of the sexes in the nesting patches of feathers or bright skin around
General Patterns of Reproductive Behavior
process and the influence of such factors the eyes or on the legs is often the
as predation, determines the degree of focus of displays (as in the blue feet of a
sexual dimorphism (differences between Blue-footed Booby [Sula nebouxii] or the
males and females) in a species. Sex- inflated pouch of a frigatebird (fig. 11.7).
ually monomorphic species show few In addition to serving to establish
differences between the sexes in external and maintain pair-bonds, courtship
plumage, while dimorphic species often displays ultimately lead to copulation
show great differences. Because of the between the breeding pair. In many
male role in territory and mate acqui- cases, only subtle differences exist
sition in monogamous birds, dimor- between courtship displays used for
phism usually results in males that are other purposes and those that end in
larger and more colorful than females. copulation. Because copulation takes
The tendency toward increases in size such a short time in most birds, it can
or brightness among males of monog- be accomplished almost anywhere.
amous species appears to be limited, Swifts are known to copulate on the

333

1stPages_B.indd 333 7/22/20 11:52 AM

 wing following display flights that take The second important value of nests
them to rather great heights, whereas is as an aid to prevent predation on the
many waterbirds copulate on the water. eggs and young. It has been suggested
Birds that use courtship feeding as a dis- that this can be done in three general
play often use it in copulation, whereas ways. Some nests are constructed such
species with display nests may copulate that the contents are defensible and the
within one of these. After all the time parent birds can actively keep predators
and energy expended in acquiring a ter- away. In other cases, the contents are
ritory and/​or attracting a mate, the effort made difficult for predators to reach, as
put into copulation among monoga- in cavities or at the ends of branches.
mous birds is generally relatively small. Finally, many nests are made as incon-
spicuous or cryptic as possible so that
Nests, Nest Building, they are difficult for predators to find.
and Nest Defense The final value of nests is to provide
optimal positioning of eggs for their
Once a pair has established itself within development. This includes influencing
a territory (either in an all-purpose terri- how the eggs bunch together so that
tory or on a nest site within a colony), it they can receive efficient heat trans-
begins preparing a nest site. The avian fer from the parents, how they can be
nest may provide at least three major turned, and how loss of eggs through
benefits, although the relative impor- rolling away can be avoided.
tance of these varies among species. To build a nest that will provide a
First, it provides thermal insulation for favorable site for egg development and
the egg, ensuring the proper heating protect against predators, the pair has to
of the egg with minimal costs for the deal with the attributes of their territory.
parent. Studies of a variety of bird nests It is obvious that pendent, woven nests
have suggested that the typical nest is do not make much sense within a grass-
equivalent to a layer of cotton of equal land habitat or on a gravel bar. Because
thickness in terms of insulative value. As nest building can take a lot of energy,
birds nest in a variety of thermal condi- the nesting birds must balance the costs
tions, these insulative properties are of of nest building with potential bene-
varying importance. Studies with hum- fits. Building a nest that is stronger or
mingbirds, where surface-area-to-volume thicker than needed may take so much
problems accentuate the costs of heat energy that less is left for laying a clutch
loss during incubation, show how nest and raising the young. Studies with the
structure depends on climatic condi- Eastern Phoebe (Sayornis phoebe) have
tions, especially temperature.13 The loca- shown that females that reconstruct an
tion of the nest may also be important old nest lay a larger clutch than females
in this regard, as selection of the proper that must construct a complete nest.15
microclimate may aid in thermoregula- Both the great variety of potential
chapter 11

tion of the egg (fig. 11.9).14 While thermal nest sites in some habitats and the
problems are most commonly encoun- apparent constraints on available sites in
tered in nesting, nests may also aid in others have led to the enormous variety
maintaining the proper humidity. of nests constructed by birds. It has been

334

1stPages_B.indd 334 7/22/20 11:52 AM

 Fig. 11.9. Variation in temperature
around a hummingbird nest during
incubation. The proper location can
reduce temperature stress (Calder 1973).

suggested that within habitats offering as dirt banks or cliffs have become home
many sites for nests, selection will favor to species with nesting habits adapted
a variety of nest types because such vari- to them, often accompanied by colonial
ation makes it harder for nest predators nesting because of the limited number
General Patterns of Reproductive Behavior
to develop a search image. Nest variation of such sites.
would also be expected because partic- The actual construction of a nest is
ular types of nest microsites (particular a compromise between the pressures
types of branches, forks in twigs, etc.) favoring insulative properties and those
would not occur in unlimited supply, favoring a cryptic, predator-free nest.
resulting in potential competition for In warm environments, selection for
nest sites. a well-insulated nest is less important,
Less complex habitats may leave and nests may be very thin to almost
fewer options for nesting, but many nonexistent. It has also been suggested
variations still occur. Among ground that the flimsy nests of many pigeons
nesters, exceedingly cryptic nests and are constructed in that way because they
eggs have evolved, while other species do not look like a nest and may thus fool
have developed the ability to construct predators.
well-hidden cup nests within short vege- Birds nesting in colonies often do
tation. Such seemingly inhospitable sites not have to deal with building a cryp-

335

1stPages_B.indd 335 7/22/20 11:52 AM

 tic nest because of the protection the were injured, attracting the attention
colony provides, although many still lay of the predator toward itself and away
eggs that are cryptically colored. On the from the nest (fig. 11.10).17 Once the
other hand, many colonial species must predator has moved a sufficient distance
deal with high densities of arthropod from the nest or young, the display
parasites. Because many of these par- is terminated. Such behaviors have
asites live in nest material, it has been been called distraction displays. Many
suggested that natural selection favors ground nesters and some birds that
simple nests among colonial birds. In a build ­floating nests cover their nests
few cases, colonial seabirds have moved with ­vegetation when they are away
their nests to trees, presumably for the from them to hide the nest. A final line
protection from arthropod parasites such of defense, found in the Common Eider
sites afford. The most extreme example (Somateria mollissima), occurs when a
of this pattern may be the White Tern female is flushed from the nest by a
(Gygis alba), which does not build a nest predator. At this time she defecates on
at all but lays its single egg directly on a the eggs with a special fluid that is quite
branch within the colony site. noxious and will repel many ­predators.
Although most nests are The behavior associated with nest
­constructed so that they are difficult for construction is highly variable among
predators to find, many have devices bird species. Usually the female plays
that discourage predators even after a dominant role in this regard, and in
the nest has been discovered. Long some species the female does all the
entrance tubes may serve this ­function, work. The behaviors associated with
as may complex tunnels within construction are sometimes extremely
the nest. The African Penduline-tit intricate; female orioles (Icterus) have
(­Anthoscopus caroli) has a collapsible been known to get trapped within their
front entrance to the tube leading to own weaving and die.
its nest. This can be closed when the
parent bird leaves the nest, so that any Incubation Behavior
visiting predator has access to only a
blind, empty tunnel.16 General patterns of egg-laying behav-
Parent birds can also reduce ior in birds were described in chapter
­predation on the nest in more active 10. The mechanism that determines
ways. In some cases, attacks on the when an individual stops laying and
predator may drive it away from the starts incubating is not fully known.
nest. These may be particularly effective Some species seem to be what are called
for colonial ­species when large n ­ umbers determinate layers; a certain number of
of birds may attack. Also noteworthy, follicles mature within the ovary each
and sometimes spectacular, are the spring, and once these eggs have been
distraction displays of many nesting laid the clutch is complete. Others are
chapter 11

birds, particularly those that nest on the termed indeterminate layers, because
ground. When a predator approaches they have the capacity to keep laying
a nest, a parent may make itself very eggs well beyond the number in a
­conspicuous and behave as though it typical clutch. In the normal situation,

336

1stPages_B.indd 336 7/22/20 11:52 AM

 General Patterns of Reproductive Behavior

these species apparently use visual or Fig. 11.10. Categories of distraction displays
tactile cues in conjunction with hor- given by birds flushed from the nest: (1) weakly
monal changes to stop laying. If eggs impeded flight; (2) strongly impeded flight; (3)
are removed from the nest as they are rodent running; (4) mobile injury feigning; (5)
laid, however, indeterminate layers will stationary injury feigning; and (6) aggressive
continue to lay eggs for long periods. distraction display (Byrkjedal 1987).
Enough variation occurs that it is not
possible to classify all species as either

337

1stPages_B.indd 337 7/22/20 11:52 AM

 determinate or indeterminate layers. ceremonies. These seem to accomplish
In most species, regular incuba- a change of incubator while minimiz-
tion begins with the completion of the ing aggression between pair members.
clutch, although as we noted earlier it In many seabirds, a pair member may
appears rather gradually with certain incubate continuously for a shift lasting
hormonal changes. Species with preco- several days. Such strong dedication to
cial young benefit if the young all hatch the eggs seems to necessitate some spe-
at about the same time, so it is best if cial display to accomplish the switching
incubation does not occur until all eggs of positions between pair members.
are laid. In many species with altricial The function of parental incubation
young, it appears that incubation may is to provide as closely as possible the
begin before the last egg is laid for optimal growth conditions discussed
adaptive reasons. In many raptors, incu- in chapter 10. Since temperature is
bation begins when the first egg is laid, usually the most variable environmen-
such that eggs hatch at intervals that cor- tal condition, most birds adjust their
respond with the intervals at which they incubation behavior with changes in
were laid. In many passerines, incuba- ambient temperature. Studies with the
tion may begin before the laying of the Great Tit show how it adjusts its time on
last egg, such that one or two eggs hatch the eggs (in terms of both number and
a day or two late. These incubation length of incubation bouts) in response
patterns often result in size variation to external temperatures to achieve
within the brood that allows the parent optimal temperature control (fig. 11.11).19
birds to “fine-tune” their production of Moisture conditions are less often a
high-quality offspring (see chapter 12). problem for incubating birds, but some
Incubation may be done by the male, species like the Egyptian Plover (Plu-
the female, or both. A survey of 160 vianus aegyptius) and sandgrouse are
families found that about 54% contained known to carry water to the eggs to raise
species where both sexes incubated, the humidity of the nest site. This is
while in about 25% only the female did.18 done by moistening the breast feathers.
The amount of male incubation is often Finally, all incubating parents must turn
negatively correlated with the amount of the eggs frequently enough that they
sexual dimorphism, as gaudy, colorful develop properly.
males may attract predators more than During incubation the parent birds
dull males. In about 6% of families only also face such problems as dealing with
the male incubates; these species often predator attacks, feeding themselves,
have mating systems other than monog- and defending their territories. All these
amy. The remaining families are too pressures must be balanced in such a
variable to classify clearly. way that the best outcome for the parent
When both members of a pair incu- birds and their young is achieved.
bate, conflict may sometimes result if
chapter 11

both want to incubate at the same time. Care and Feeding of Young
For this reason, and perhaps also for
pair recognition among colonial nesters, With the hatching of the eggs comes a
some species have ritualized nest relief shift from the rather leisurely activity

338

1stPages_B.indd 338 7/22/20 11:52 AM

 of incubation to the rigorous activities Fig. 11.11. Incubation rhythms of the Great
associated with the care of nestlings. As Tit in relation to external air temperature.
with other reproductive activities, hor- Note that birds incubate longer when it is cold
mones seem to set the stage for feeding (Kluijver 1950).
and other behaviors, some of which may
appear before the eggs hatch. In most
cases, however, it is the final stimulus must both feed and brood the nestlings
offered by the hatched young that leads early in life, during which time the nest
General Patterns of Reproductive Behavior
to the parents gathering and bringing site is exposed to predation. When faced
food to the nest and undertaking other with potential predators, many birds of
parental duties. both altricial and precocial species will
Parental care of nestlings involves perform distraction displays such as
feeding and protecting the young as well those discussed earlier. As altricial young
as keeping them warm, usually through develop to the point where they can main-
brooding behavior (which is much like tain their own body temperature, parental
incubation but occurs after hatching). energy can be diverted to activities other
The relative importance of such behav- than brooding. Species with semipreco-
ior varies with the species. Obviously, cial or semialtricial young (chapter 10)
birds with precocial young that can are intermediate between precocial and
feed themselves and thermoregulate altricial species in the amount of brood-
spend less effort gathering food and ing or feeding required, based on the spe-
brooding, but more time looking out cific adaptations of the species regarding
for predators. Birds with altricial young down feathers or mobility.

339

1stPages_B.indd 339 7/22/20 11:52 AM

 An important behavioral adaptation directing food into the nestling. This very
in many precocial species is imprinting. simple but critical gaping behavior in
Imprinting is the fixation of a young nestlings can be stimulated in a variety
bird on its parent, such that it follows of ways, depending on the species. In
the parent about and therefore can many cases, any motion that stirs the
respond to parental commands and nestling, such as touching the nest or
receive parental care. A strong impulse nest branch, will trigger this response.
to follow the parent needs to be pack- In some cases, vocalizations seem to be
aged within the behavioral repertoire the primary cues, such that the parents
of a young precocial bird to increase require begging calls from the young
its chances of survival. In most cases, to be stimulated into gathering food. In
imprinting occurs in the first few hours some species, the young will not open
after birth, and because at least one their mouths unless they hear the proper
of the parent birds is there, the baby call from their parent. In such species
imprints on a parent. Once this object is as gulls, marks on the bill of the parent
imprinted, it remains fixed through the seem to be critical in eliciting the proper
development of the young. If for some feeding behavior in the young. Most of
reason the parent is not there, a baby the studies done on this behavior have
bird can imprint on a variety of objects; shown that a baby bird responds most
generally the largest moving object in strongly to the colors of its parent’s
the area is chosen. Great variation in bill. This is quite obviously an innate,
imprinting occurs, with the young of species-specific characteristic, and
some species selecting objects resem- ethologists have learned much from the
bling their parents, while other young variation in this genetically programmed
seem to have little discriminatory ability. behavior.20 These cues may sometimes
Among the classic examples of mis- work in combination, and they may vary
directed imprinting are domestic geese through the development of the young.
that have imprinted on their owners, or For example, it appears that both calls
grouse that have imprinted on tractors. and bill marks are important among
Imprinting mistakes often result in many colonial gulls. The calls are used
completely abnormal birds because of by the parents and young to identify one
the crucial role of learning from con- another individually, while the bill marks
specifics in the development of proper elicit the final feeding response. In many
foraging behavior, mate selection, and species that use vocal or tactile stimuli
other important group interactions. for the feeding response early in life, the
Cues that initiate feeding by the development of vision allows visual cues
parents and that synchronize interaction to function later in life.
between parents and young come from There is evidence that the interac-
a variety of sources. In many species tion between parents and young during
the young have very bright mouthparts, feeding also affects the effort a parent
chapter 11

particularly the gape, which serve as puts into food gathering. The gaping or
strong stimuli to the parents. In some begging behavior of an individual does
cases, the interior of the gape has tar- not occur for a period following feeding,
get spots or other markers that aid in so if all the young are fed regularly the

340

1stPages_B.indd 340 7/22/20 11:52 AM

 parent is exposed to relatively few beg-
ging behaviors at each feeding visit. This
may affect the intensity of foraging in
the parent. Experiments with Pied Fly-
catchers (Ficedula hypoleuca) in specially
designed nest boxes have been able to
manipulate the amount of parental feed-
ing by changing the number of young in
the nest or by deception.21 In this latter
case, a single nestling was exposed to
the parents but other young were kept in
the back of the box such that the parents
could hear their calls when feeding the
single young. As a result of this stim-
ulation, the parents brought in much
more food than they normally would to
a single offspring.
This interaction between parents
and young may also help explain the
general increase in feeding rates as the
young grow, as the older young may
stimulate their parents to greater activity
(fig. 11.12).22 All this stimulation can
result in rather impressive numbers
if one goes to the effort of watching
parents feeding their young. Great Tits
have been estimated to make up to 900
visits to their nests with food each day,
while most small birds make 300 or 400
General Patterns of Reproductive Behavior
trips daily. In contrast, raptors may get
sufficient food to their young with only Fig. 11.12. Variation in feeding rates of
a trip or two daily, although each trip Mountain Chickadees (Poecile gambeli)
may provide a large food item such as a through the nesting period: (top) variation in
rabbit or bird. Male and female roles in daily visits; (center) variation in prey volume
the care of nestlings vary greatly among delivered by trip; and (bottom) increase in size
monogamous species. Much of this of prey items over time (Grundel 1987).
variation may depend on the amount of
brooding done by the female, especially
if only the female has a brood patch.
When the female does the brooding,
the male must provide much more food
than his mate. If both sexes can brood,
more equitable division of labor may
occur, although other factors may affect

341

1stPages_B.indd 341 7/22/20 11:53 AM

 this. Studies of many species suggest ularly as the young get older, this food is
that females generally feed their young whole and is carried to the young in the
more often than males, but males may parents’ bill. In others, the food may be
bring in larger food items or larger eaten by the parents, partially digested,
amounts of food (perhaps because of and then fed to the young. This process
optimal foraging factors related to the provides several potential benefits. The
male’s generally larger size). In hawks, partial digestion of food by the parents
the female broods the young and feeds may ease digestion for the young and
them by tearing apart the food items may even provide them with some
brought to the nest by the male. Female digestive juices. Eating the food also aids
hawks do not forage for food until the the parent in flying, as it allows the food
young are old enough to stay warm and to be closer to the center of gravity than
feed themselves. it would be if carried in the bill. This
The foods fed to nestlings vary may be critical to birds such as seabirds
in much the same way that parental that travel long distances with food.
foods vary (see chapter 4), but there In some cases, the parent goes
is a general increase in the amount of beyond just partially digesting the food
protein fed to young, usually through to converting it into a liquid food sub-
the use of insects as food. Species that stance. Although the “pigeon’s milk”
feed mostly on fruits or other vegetable that pigeons feed their young is best
matter generally cannot feed these items known in this regard, many other
to their young but must catch insects for species, especially seabirds, feed their
them or, in the case of precocial young, young some sort of secreted meal.
take the young to locations where the The process of feeding may be
young can catch their own insects. It has accomplished by either the parent shov-
been shown that a young Ruffed Grouse ing food into the throat of the young, or
(Bonasa umbellus) will eat about 90% the young bird shoving its bill into the
insects and 10% vegetable matter during throat of the parent (fig. 11.13). Species
May, but nearly all vegetable matter by with rather intricate feeding maneuvers
August. In some cases, these shifts in often have distinct markers that help
diet reflect stages in the development both parent and nestling synchronize
of the bird’s intestinal tract. Studies in the feeding effort.
which nestlings were fed diets com- The tremendous amount of food fed
posed largely of fruits or seeds with few to a nestling means that there will also
insects showed pronouncedly reduced be a tremendous amount of waste mate-
growth rates among these young (see rial. In nearly all species (some pigeons,
chapter 10). trogons, and motmots are exceptions),
The parents of precocial species do this material is removed to keep the nest
not directly feed the young, but they tidy. A clean nest probably attracts few
must lead the young to areas where they predators and keeps the young dry and
chapter 11

can catch enough food. Food for altricial warm, and free of parasites or disease.
young must be brought by the parent to In some species, nestlings defecate
the young bird. In many species, partic- over the side of the nest early in life,

342

1stPages_B.indd 342 7/22/20 11:53 AM

 General Patterns of Reproductive Behavior

Fig. 11.13. A baby Brown Pelican (Pelecanus

occidentalis) being fed by a parent. ier, most feces of nestlings occur as fecal
sacs, droppings with membranes that
allow the parents to carry them away.
which may result in a pile of droppings Some species drop these specifically
below the nest. When the nest is vul- into water, while others just drop them
nerable to the predators that might be at some distance from the nest. In some
attracted by such a pile of droppings, cases, particularly early in the nestling
adaptations have developed to remove stage, the parents may eat the fecal sacs.
these droppings. To make removal eas- Presumably this is because the imma-

343

1stPages_B.indd 343 7/22/20 11:53 AM

 ture digestive tract is inefficient enough young for long periods. Some seabirds
that the parents can still get energy from feed their young up to six months of
these waste products. It has been esti- age, during which time they may have
mated that up to 10% of a parent’s daily migrated thousands of miles. In spe-
energy might be gathered in this way. cies with rather sophisticated foraging
behavior, such as many predators, the
Fledging postfledging period may be important in
teaching the young birds how to cap-
As noted in chapter 10, most young birds ture prey. In many cases, it appears that
rapidly develop into adult-sized birds. At the young are allowed to stay with the
this time they are ready to leave the nest, parents until the next breeding season,
a process known as fledging (at which at which time the union is dissolved
time they are called fledglings). Preda- or the young are chased off the paren-
tion pressures favor the earliest fledging tal territory. In species with precocial
possible, while growth-related factors young, such postfledging care would be
favor later fledging. While most young of little utility, although the parents and
birds approach adult size at the time offspring may remain together because
of fledging, species like cuckoos fledge of the advantages of flocking. In some
when they are much smaller than adults. Arctic shorebirds, the parents leave the
In these cases, the development of wings offspring when they are still unable
and flight feathers proceeds faster than to fly, which means that these young
that of other parts of the body. mature and find their way to the winter-
The fledging process often takes ing grounds without parental assistance.
some coaxing from the parents. Some- The desired result of this parental effort
times the parents stop feeding the is an independent offspring that will be
young, presumably so that hunger will capable of breeding in subsequent years.
drive the young out of the nest. In other To this point, the focus has been on
cases, the parents may entice the young general patterns of reproductive physi-
away from the nest by showing them ology and behavior, using monogamous
food items but not actually feeding them. birds as a standard model. Variations
The amount of parental care after within these standard patterns are
fledging varies greatly. In many mul- examined in chapter 12, and the ecolog-
tibrooded species, the female starts to ical conditions favoring these variations
lay a clutch of eggs as soon as the first are noted. All these variations reflect the
brood fledges, such that only the male evolutionary process as it favors adap-
provides postfledging care. In other spe- tations that maximize reproduction in
cies, both parents help take care of the different environments.
chapter 11

344

1stPages_B.indd 344 7/22/20 11:53 AM

 C HA PT E R 12

Adaptive Variation
in Avian Reproduction

T
he previous two chapters have to reproduction, many birds seem to
focused on the mechanis- produce young at some lower rate. Evo-
tic aspects of reproduction, lutionary biologists tend to think of this
especially the physiological reduction as an adaptive compromise
and behavioral adaptations needed to that balances a variety of factors other
produce eggs and young. Physiolog- than just the absolute number of young
ical and behavioral factors also serve that can be produced at a particular time.
as constraints on the number of off- This chapter examines the variation that
spring birds can produce. Incubation, occurs in birds in producing an optimal
the energy needed for egg production, number of young rather than the num-
and the time required to find food for ber that may be physiologically possible.
altricial young all put limits on the Throughout this chapter we will
maximum number of offspring a pair assume that reproductive characteristics
of birds can raise at a time. If we look at are the products of natural selection.
the actual reproductive characteristics For this to be the case, reproductive
of birds, however, we see a great deal traits must be inherited through genetic
of variation, both among and within means and natural selection must favor
species. For example, a House Wren those individuals with particular repro-
(Troglodytes aedon) that lives in Panama ductive traits. For example, for clutch
usually lays two or three eggs per clutch, size to be an evolved trait, offspring of a
whereas one breeding in Canada may female must have the genetic propensity
lay up to seven eggs. A duck nesting in to lay clutches of the same general size
the Arctic may lay a clutch of eight to as their mother. In this way, an initial
ten eggs, whereas a seabird in the same population of females might exist with
region may lay only one egg. the genes to lay a variety of clutch sizes.
These examples suggest that many Natural selection will then favor those
birds are responding to evolutionary and females that lay a clutch of a particular
ecological factors that result in reproduc- size, while females laying either more
tive efforts smaller than purely physio- or fewer eggs will not reproduce as well
logical or behavioral constraints might (see below for more details on this). If
allow. In other words, while physiology clutch size is not a heritable trait, natural
or behavior might set maximal limits selection cannot operate in this manner.

345

1stPages_B.indd 345 7/22/20 11:53 AM

 To date, studies have indicated that vir- less, the concept of strategies is some-
tually all reproductive traits, while show- times a good way for us to look at how
ing some variation with age or breeding birds respond to the variety of condi-
condition, have basic genetic compo- tions in which they attempt to breed.
nents that are passed from generation to
generation. Therefore, all reproductive Bird Populations and Their
traits are considered to be evolved traits. Reproductive Correlates
As the conditions that promote Population fluctuations
various options in reproductive behavior
are examined, it must be remembered In studying bird populations it is usually
that this variation occurs because a impossible to count the total number
subset of individuals with a particular set of individuals of a particular species.
of genetic traits produces more young Rather, the number of birds per unit
under those ecological conditions than area, or density, is studied. As a general
individuals with other genetic traits. That rule, if a habitat does not change sig-
is the essence of natural selection. In nificantly from year to year, the density
many cases we will try to explain a partic- of birds in that habitat at a particular
ular situation by asking questions about time of year will also be very consistent.
possible options: Does a female that lays This stable population level for a species
two eggs produce more surviving young within a habitat is generally identified as
than a female that lays four eggs? While the carrying capacity of that habitat, as
the answer is the result of selection it suggests that at that point the habitat
favoring either two- or four-egg clutches, is sufficiently full of the species that no
many scientists like to approach such more individuals can be supported.
questions by asking themselves what the Recent work with tropical birds
best strategy for a female would be under suggests exceedingly stable populations
particular circumstances. (fig. 12.1),1 while long-term studies with
Under this approach, one might ask: birds in temperate climates show some
What is the best egg-laying strategy for a fluctuations around an average popula-
female House Wren in Panama? When tion level. This consistency in density
is sharing a male mate a better strategy suggests that some factors must be at
than monogamy? When is a bird help- work regulating these populations, and
ing its parents a better strategy than it the differing stability of populations in
attempting to breed itself? Whereas the tropical and temperate zones suggests
conditions in which a strategy is most that climate must play a role in this reg-
effective may be identified by looking at ulation. If we follow these same popula-
the ecological and evolutionary situation tions through the year, we see seasonal
in which the behavior is found, it must variation because of the production of
always be remembered that birds do young. This seasonal variation is also
not actually have conscious strategies generally greater in the temperate zone
chapter 12

in these reproductive behaviors. Rather, than it is in the tropics.

they show a variety of behaviors, and Under undisturbed conditions, most
natural selection chooses those that populations of a species show fairly
work best in those conditions. Neverthe- limited variation in size throughout

346

1stPages_B.indd 346 7/22/20 11:53 AM

 Fig. 12.1. Variation in resident bird density on
the expansion of a species into a new
Barro Colorado Island, Panama, through the
habitat. Habitat modification in the New
year. Note how stable resident populations are
compared to migrants (Willis 1980). World has certainly increased the popu-
lations of such species as the American
Robin (Turdus migratorius), which does
well in suburban habitats. Introduced
their range. Some populations fluctuate species such as the European Starling
greatly on a local scale. For example, (Sturnus vulgaris) and Ring-necked
in chapter 9 we discussed how cer- Pheasant (Phasianus colchicus) have also
tain seed-eating birds from the north shown great population increases in
occasionally invade southern areas in some areas. In general, however, these
massive irruptions because of crashes populations have eventually stabilized
Adaptive Variation in Avian Reproduction
in their northern food supplies. While as they increased to match the available
these may seem to be unstable popula- habitat (thereby reaching carrying capac-
tions, if we consider these species’ pop- ity). Thus, observed over long enough
ulations on a larger scale, they probably periods or on the proper regional scale,
do not vary as greatly as we might think. even the seasonal fluctuations of most
Truly irruptive populations probably bird populations suggest some form of
occur only in very seasonal habitats such regulation rather than just drastic popu-
as some deserts, where drastic fluctu- lation expansions and crashes.
ations in food supply and other factors
occur over periods of many years, and Population regulation
many species are unable to migrate to
other locations. Factors that can regulate bird popula-
Other noteworthy changes in pop- tions come in two general categories.
ulations reflect changing conditions or Density-independent factors are those

347

1stPages_B.indd 347 7/22/20 11:53 AM

 that operate, as the name implies, inde- by density, at which time density-de-
pendently of the density of the species. pendent limitation would occur. On the
Climatic factors such as cold or rain are other hand, density-independent fac-
the chief density-independent factors; tors may reduce populations with such
the lowest temperature in winter is obvi- regularity that they rarely reach densities
ously not a function of the number of great enough to show density-depen-
sparrows living in a habitat, although it dent limitation. Often, the overall effect
certainly may affect that number. Trying of density-independent factors such as
to understand the population levels of extreme climatic conditions is a func-
species affected by density-independent tion of a species’ density. A cold, harsh
factors is largely a matter of trying to winter may cause more deaths when
understand how each species deals with populations are high than when they are
fluctuations in its general environment. already low for some other reason.
Density-dependent factors, on Several correlations occur between
the other hand, affect individuals in a the patterns of change in population
variable way that depends on population size and the relative importance of
density. When populations are low, these density-dependent or density-indepen-
factors may be relatively unimportant, dent factors, and these relationships
but as populations increase they have a greatly affect the general patterns of
greater effect. Food is perhaps the most reproduction in birds (fig. 12.2).2 Popu-
obviously density-dependent factor, but lations that vary little from year to year,
other factors that affect density depen-
dency may include competition, preda-
tion, roosting or nesting sites, disease,
Fig. 12.2. General comparison of annual
and so forth. resource and/​or population variation in a
Factors from these two general stable tropical habitat (left) and the temperate
categories obviously interact, for in the zone (right). The amount of variation between
absence of any density-independent maximum and minimum levels accounts for
limitation, populations would grow until much of the difference in reproductive traits in
food or some other factor was limited the birds frequenting these regions.

348

1stPages_B.indd 348 7/22/20 11:53 AM

 or even within a year, tend to suffer ments. A bird in a tropical habitat is
little from density-independent factors not exposed to harsh winter conditions
(often because they live in stable, mild that may cost it its life. Rather, once this
climates) but are subject to relatively bird has reached adulthood it has a high
high levels of density-dependent limita- probability of a rather long life span.
tion. The tropical populations discussed During this life, though, it must deal
earlier are rarely subjected to cold or with a variety of limitations caused by
other extreme climatic conditions; thus the number of conspecifics with which it
they fluctuate little and their carrying must live and the diversity of other spe-
capacity is determined primarily by cies that live in this stable climate, many
density-related factors. Temperate-zone of which may serve as predators, com-
populations are reduced nearly every petitors, or parasites of the bird. While
winter by factors associated with harsh the bird may live a long time under
climatic conditions (a density-indepen- these conditions, it may find gathering
dent factor). Each spring, populations enough extra food for its young difficult,
are below the carrying capacity of the which may limit the number of young.
habitat such that density-dependent fac- Natural selection may also work against
tors are relatively less important through behavior that involves risking its future
the breeding season. life span with small chances for reward.
As a general approximation, this Such risk-benefit trade-offs may limit
difference between the effects of densi- how often or where a bird nests. The
ty-independent factors in tropical and result may be an individual that breeds
temperate habitats explains some of the infrequently and produces only a few
differences in reproductive character- young at a time, although this is enough
istics in these regions. Certainly, if we to match the low mortality rates under
compare a standard temperate-zone pop- these conditions.
ulation typified by rather great seasonal In contrast, a bird living with sub-
fluctuations in density with a more stantial density-independent population
stable tropical-zone population, it should control faces a decidedly different set of
not be surprising that temperate-zone circumstances. Even if it is successful
Adaptive Variation in Avian Reproduction
reproduction is characterized by greater in reaching adulthood and breeding
production of young than in the tropics. condition, it generally does not live a
Temperate-zone species have the poten- long time. When it is time to breed,
tial to increase populations severalfold though, an almost unlimited supply of
during the breeding season through food may be available because popula-
such means as large clutches or multiple tions of nearly all species are well below
breeding attempts. Because total densi- carrying capacity as a result of the effects
ties rarely differ from near the carrying of winter. This means that the bird can
capacity of the habitat, tropical species find enough food to feed many young,
are less likely to show such characteris- and the chance that it may not live to
tics of high productivity. breed again means that it should take
Mortality factors must also be more risks to maximize each breeding
examined in understanding reproduc- attempt. The general result is a temper-
tive characteristics in different environ- ate-zone species that may breed often

349

1stPages_B.indd 349 7/22/20 11:53 AM

 and have large clutches; this, too, tends ingly, birds in environments with fluctu-
to result in similar numbers of birds ating populations generally breed earlier
of this species at a particular time each in life than those of stable environments
year, but the life history traits of this (i.e., seabirds or tropical species).
temperate zone bird are very different Once a bird has started breeding,
from those of its tropical relative. reproductive success can be affected by
egg size, clutch size, and the number of
Reproductive options broods in a season. Egg size is somewhat
variable within a species, but it is most
For an individual to maximize its genetic often affected by the precocial-altricial
impact on the population, there are factors discussed earlier. We will discuss
several sets of options for life history and clutch size in detail later; it and the num-
reproductive characteristics. Survival to a ber of broods in a season are affected by
future breeding season is important, but the same general factors. Also important
in most cases a bird has relatively little in some cases are the rate of develop-
control over factors affecting its mortal- ment of the young and the amount of
ity. In a temperate environment, a bird postfledging care they require. These lat-
can do fairly little because climatic fac- ter factors particularly affect the number
tors tend to control its fate, while in the of broods that can be reared in a season.
tropics a bird might avoid certain poten- Species with long development times
tial risks or not take certain chances, but that live in very seasonal environments
this cannot guarantee against falling prey can be flexible only in clutch size, once
to a hidden snake or tropical disease. the age of first reproduction is reached.
Although little can be done to For this reason, we will spend more time
change mortality factors, several options discussing this factor.
can affect reproductive rates. The age at Although we can attempt to under-
which the first reproduction occurs can stand the ecological factors that work
greatly affect reproductive potential. In on a single reproductive characteristic
most birds, first reproduction occurs at (e.g., clutch size), it is difficult to separate
about one year of age, primarily because totally the various life history traits of a
of the seasonal nature of reproduction. species. In the example above, the stable
Some birds have been known to breed conditions of tropical environments,
at just a few months of age, particularly long life, and low reproductive rates are
among finches in erratic environments all interrelated, as are the temperate zone
such as deserts.3 In larger species, the characteristics of unstable conditions,
age at first reproduction is often much shorter life, and higher reproductive
more than one year, and many large rates. What can be considered a stable
birds of prey or seabirds do not breed or unstable environmental condition
until nearly 10 years old. In some is also variable; a large predatory owl
cases of delayed age of reproduction, it in a particular habitat may respond as
chapter 12

appears that the bird is physiologically though it is a stable environment, while

capable of breeding at one year of age, small seed-eating birds may experience
but environmental factors do not allow the same habitat as an unstable environ-
breeding until later in life. Not surpris- ment. Potential life spans vary with the

350

1stPages_B.indd 350 7/22/20 11:53 AM

 size and type of bird in a way that affects of birds for a variety of reasons. It is
general patterns of life history traits. a discrete entity, involving only the
Finally, the idiosyncrasies of some spe- number of eggs in a nest, and the eggs
cies will provide exceptions to almost any are generally presumed to come from
generalization we might make regarding the parent(s) that constructed that nest.
patterns of avian reproductive behavior. Since many species nest only once a
Nonetheless, some general state- year, if that nest is successful, it is the
ments can be made about the variation best estimate available of annual repro-
in life history parameters and reproduc- duction. Clutch size also varies greatly,
tive characteristics in birds. As these both within and among species, which
general statements are made, remember allows for studies on the effects of envi-
the relative nature of these comparisons. ronmental factors in the evolution of
Thus, the temperate-dwelling owl in the clutch size. Finally, clutch size is import-
example above has more stable popula- ant because it can be easily manipulated
tions than the finch living in the same (by adding or removing eggs) in ways
habitat and may therefore have relatively that other reproductive traits cannot.
lower reproductive rates. If we compare To understand the factors (other
this owl with a conspecific living in the than physiological constraints) that
tropics, however, the tropical individual affect variation in clutch size, we must
most likely belongs to an even more first look at how various factors are bal-
stable population and thus has an even anced to produce an optimal clutch size
lower reproductive rate. for a region. With this knowledge, the
Within the tropics, we might expect variation that occurs among species is
relative differences between very stable clearer, which also aids the understand-
habitats such as rainforests and seasonal ing of regional variation within species.
habitats such as thorn forests or savan- This section ends with a look at some
nas. In all this variation, we must always adaptations of species living in variable
remember that reproductive character- environments.
istics seem to be correlated best with
population characteristics, such that The optimal clutch size for
Adaptive Variation in Avian Reproduction
relatively long-lived birds with relatively a regional population
stable populations both among and
within years tend to produce young at It can generally be said that the optimal
a rate relatively lower than that of birds clutch size is the one that leaves the most
with populations that are more variable offspring in subsequent generations. For
among and within years. In the next a small population living in a particular
section, we will take a more detailed look habitat type, it seems that those indi-
at the way clutch size enters into these viduals that produce the most offspring
general patterns. (within any physiological or behavioral
constraints) will most affect the gene
Clutch Size Variation pool of subsequent generations. The
key here, as in any situation, is that the
Clutch size has been one of the most offspring must survive long enough to
intensively studied reproductive traits breed. If the production of many nest-

351

1stPages_B.indd 351 7/22/20 11:53 AM

 lings results in poor-quality offspring, Even though this one offspring might
few of these offspring may survive long have an excellent chance of surviving to
enough to breed and the trait for large breed in the future, parents that produce
clutch size is therefore not passed on two or more offspring that are healthy
to future generations. Thus, it appears enough to survive to breed will contrib-
that in any habitat there is some balance ute more genes to subsequent genera-
struck between producing the maximum tions than the parents of a single supery-
number of young and producing young oung. To the extent that clutch size is
of a high enough quality that they have a genetically determined, a clutch of more
chance of surviving to breed. than one will be favored.
The quality of offspring is strongly The average clutch size for a region,
related to how much food they receive, then, is the balance struck between pro-
particularly in altricial birds. If fed well, ducing the largest number of young pos-
young birds can develop properly and sible and ensuring that these young are
reach adult size rapidly, both of which healthy enough to have a good chance of
may increase their chances of surviving surviving to breed in the future. A clutch
into the future. If we think of parent that is too large may leave few surviving
birds as having a maximum amount offspring, while one that is too small will
of food that they can bring to a brood, be outnumbered genetically by those
adding an egg to a clutch divides this individuals producing more young. We
amount by some increment. This may assume that a balance between these
affect the growth rate of the young. two factors occurs for each species in
Studies with the Great Tit (Parus major) each region to lead to the evolution of a
have shown that clutch size tends to be particular clutch size for that population.
inversely related to the weight of the Such a mechanism does not mean that
fledglings (fig. 12.3);4 individuals with a specific clutch size is fixed within the
large clutches produce lighter young. population. Rather, factors related to age
In some cases, these lightweight young or experience, food supply (from climatic
do not develop properly and do not even variation or population fluctuations), or
fledge. In other cases they may be able seasonal variation may result in some
to leave the nest, but studies with several variation around an average clutch size
species (including the Great Tit) have (fig. 12.3). In species that live in envi-
shown that in general, smaller offspring ronments that vary greatly among years,
have lower chances of surviving to reach clutch size variation may be adaptive.
breeding age. This suggests that birds For example, particularly dry years may
producing relatively large clutches do favor individuals with smaller clutches
not leave as many breeding offspring in than average, while wet years may favor
subsequent generations as those produc- those with larger clutches, resulting in a
ing somewhat fewer, but larger, young. variable clutch size within the species. In
Given that the quality (health) of the species living under relatively predictable
chapter 12

young is important, we should consider conditions, however, great variation in

the effects of producing just one, very clutch size should be selected against.
healthy offspring on an individual’s
potential contribution to the gene pool.

352

1stPages_B.indd 352 7/22/20 11:53 AM

 Clutch size variation among species Fig. 12.3. Clutch size evolution in the Great
Tit (Parus major). Larger broods have lighter
If we assume that the optimal clutch young (upper left), and heavier young generally
size for each species is determined by live longer (upper right), but there is a balance
this balance between the quantity and between weight and survival that suggests that
quality of offspring, the differences producing a medium-sized brood of medium-
sized young is the best strategy overall (bottom
among species in clutch size should
left) and produces the optimal clutch size for
be related mostly to the factors that
that region (bottom right) (Perrins 1965, 1980;
determine offspring quality. Since in Perrins and Moss 1975).
most cases this is food supply, it is not
surprising that the availability of food

353

1stPages_B.indd 353 7/22/20 11:54 AM

 for the young seems to be the chief duce precocial young, but the require-
determinant of interspecific clutch size ments of a large egg coupled with the
variation. Species feeding on foods that small body of the incubating parent
are rare or widely distributed will be apparently limit clutch size greatly. A
able to raise fewer young than species large pheasant or duck does not face this
feeding on abundant foods. In general, limitation. In many species with very
large foods are less abundant than small small clutches, physiological or behav-
foods, so we might expect large birds to ioral limitations may be operating, as
have smaller clutches for this reason. increasing the clutch by even one egg
Additionally, birds with young that feed may result in severe losses among all
themselves (precocial birds) should have the young. For example, swifts living in
more young than birds in which the par- the same general area as Great Tits lay
ents must provide all the food, all other only two or three eggs, and the addition
things being equal. of a single egg may cut the number of
The clutch sizes of a variety of avian fledged offspring (fig. 12.4). Swallows,
groups are shown in table 12.1. It is not however, which have very similar gen-
surprising that seabirds and raptors eral food habits and share many habi-
have relatively small clutches compared tats with swifts, have appreciably larger
to those of small insectivores or birds
with precocial young.
While our model of optimal clutch Fig. 12.4. Fledging rates in relation to clutch
size helps explain all these differences, size in swifts. Normal clutch size was two or
in a few cases other constraints appear three eggs, but artificial clutches of four were
to be operating. For example, small laid. Note the reduced production of young in
shorebirds (sandpipers and the like) pro- these enlarged broods (Perrins 1964).
chapter 12

354

1stPages_B.indd 354 7/22/20 11:54 AM

 clutches. Most seabirds lay only a single Table 12.1
egg, and adding a second may result in Examples of typical clutch sizes
the loss of both young. within ­different types of birds
Predation pressures may play some number
role in interspecific differences in clutch group
of eggs
size, particularly in differences between Penguins 1–2
hole-nesting and open-nesting birds. Loons 2
It appears that those species nesting in
Grebes 3–6
relatively predator-free locations such as
Procellariiformes 1
cavities lay larger clutches than similar
Pelicans and cormorants 1–4
species that use open nests. Predator
Herons and egrets 3–5
pressures may also affect clutch size
Geese and swans 3–6
limitations among open-nesting birds,
Ducks 7–12
particularly among ground-nesting birds
Hawks, eagles, and vultures 1–5
with large clutches of precocial young.
Grouse, pheasants, quail, and 5–18
The longer it takes to lay and incubate
123ptarmigan
eggs, the greater the chance of a preda-
Cranes 2
tor finding the nest. At some point, the
Rails, coots, and allies 5–12
chances of predation may outweigh the
Shorebirds (sandpipers and 3–4
benefit of a larger clutch. Within the allies)
same habitat when we look both among Gulls and terns 2–3
and within species, it is hard to measure Auks 1–2
the predation factor, except in the case Pigeons and doves 2
of a predator finding the nest as noted Owls 2–7
above. (The role of predation in intra-
Nighthawks and nightjars 2
specific variation on a geographic scale
Swifts 1–5
is discussed below.)
Hummingbirds 2
This leaves a variety of factors that
Woodpeckers 3–6
may affect the evolution of clutch size
Antbirds 2–3
when all species are considered. Yet the
Manakins 2 Adaptive Variation in Avian Reproduction
effects of body size, population param-
Tyrannid flycatchers 2–6
eters, food supply, predator pressures,
Swallows 3–7
and the developmental type of the young
Birds of paradise 2–3
help explain the general patterns dis-
Chickadees and titmice 4–15
cussed above.
Wrens 2–11
Old World warblers 2–10
Variation in clutch size within species
White-eyes 2–5
Sunbirds and honeyeaters 1–3
We have already pointed out that the
Orioles and blackbirds 2–6
House Wren may lay two or three eggs 123(Icterinae)
in the tropics and up to seven in the Goldfinches and allies 3–6
temperate zone. Geographic variation Estrildid finches 4–10
in mean clutch size has been found in
numerous species along a variety of

355

1stPages_B.indd 355 7/22/20 11:54 AM

 Fig. 12.5. Relationship between latitude and purposely “balancing mortality.” While
clutch size for members of the Old World it may be true that reproductive rates
genus Emberiza (left) and members of the tend to match mortality rates (see below),
New World blackbird family (Icteridae) (right). this pattern is more a result than a cause
Orange dots (left) and green dots (right) show of clutch size patterns. Modern evolu-
cavity-nesting species (Cody 1966). tionary theory provides no mechanism
by which a bird may choose to balance
­ radients. Much of the work that has
g mortality (early arguments favoring this
looked at latitudinal gradients in clutch hypothesis require some form of group
size (fig. 12.5)5 has shown that most selection). Another explanation suggests
temperate birds lay larger clutches than that day length is the critical factor,
their tropical counterparts. as a temperate bird has much more
Similar patterns have been shown time each day to feed its young than its
along longitudinal gradients from tropical counterpart. While this extra
coastal areas to the interior of conti- time certainly does not hurt, it does not
nents, and with altitude (with lowland explain altitudinal or longitudinal pat-
birds having smaller clutches than terns. Additionally, nocturnal owls show
montane species). Many populations on the same latitudinal patterns as other
offshore islands have smaller clutches species, even though their foraging time
than their mainland counterparts, while is at its minimum during the breeding
species in more seasonal habitats in the season in the North Temperate Zone.
tropics have larger clutches than those The “spring bloom” hypothesis sug-
of nearby, less seasonal habitats. gests that the increased productivity of
A variety of explanations have been the temperate zone allows much larger
offered over the years to explain these clutches; while this does appear to help
patterns. Some have suggested that phys- explain some of the variation, changes
iological limits cause these patterns, but in productivity seem to be only loosely
chapter 12

many experiments have shown that this related to clutch size variation. Finally,
is not the case. Because small clutches the predation hypothesis suggests that
often occur in more stable environments, species in the tropics have smaller
it has been suggested that the birds are clutches because tropical environments

356

1stPages_B.indd 356 7/22/20 11:54 AM

 have larger numbers of nest predators. feeding of young. Tropical environments
Large clutches (and hence large broods) have stable populations and high species
might attract nest predators more than diversity. Competition is therefore high
small broods because the parents must and food relatively hard to find. With
feed large broods more often, thereby the spring bloom, decimated popula-
assisting the predator in locating the tions following winter, and relatively
nest. Many studies have suggested that low species diversity, temperate species
nest predation rates are much higher should have to spend less energy finding
in the tropics than in the predator-poor a similar amount of food.
temperate zone. On the other hand, The dependent variable in this
species such as hole nesters that are model is the allocation of energy to
relatively immune to nest predation still clutch size. If we examine two species
show latitudinal gradients in clutch size, with similar amounts of total available
as do the predators themselves. energy, a tropical species might need
While none of the above hypotheses to spend more of its energy in predator
can really explain geographic variation avoidance (including building a better
in clutch size, it is obvious that many nest) and more in food gathering than
of them have some validity and that a temperate species, leaving less energy
some combination of factors is at work for investment in clutch size. Thus, it
in determining clutch size. Although would produce a smaller clutch than a
several models have been proposed that species in the temperate zone, where
depend on combinations of factors, the less energy had to be allocated to preda-
author’s favorite is that of Martin Cody. tor avoidance and food gathering.
He developed a model using the princi- Although the Cody model was
ple of allocation (the idea that a bird has designed to explain latitudinal gradients
a limited amount of energy that it must in clutch size, it is general enough to
allocate in an optimal way to produce explain clutch size variation in almost
offspring). He proposed that clutch any situation in which stable environ-
size is determined by the interaction mental conditions are compared with
of three factors, one related to predator less stable conditions. Energy invest-
Adaptive Variation in Avian Reproduction
avoidance, one to food supply, and one ments in relatively stable situations
to the allotment of energy to clutch size. where populations are near carrying
Predator avoidance considers a bird’s capacity all the time can be compared to
chances of losing its nest and any risk those in situations where populations
the bird might take while nesting. In vary greatly. As it turns out, all the gradi-
temperate birds, the allocation of energy ents described earlier (latitudinal, coast-
to this factor is generally low, as preda- al-interior, longitudinal, altitudinal, and
tion rates are relatively low, while the island-coastal) are gradients of environ-
reverse is true in the tropics. Elements mental stability. Where populations vary
of the predation hypothesis mentioned little from carrying capacity, more energy
above apply here. must be allocated to the predation and
The food factor in this model food axes. Where they vary greatly, more
considers the amount of food available energy is left to allocate to large clutches.
to a species for egg formation and the The beauty of this model is that we

357

1stPages_B.indd 357 7/22/20 11:54 AM

 can see that a change in allocation of one clutch in one year may be too big or
factor affects at least one of the other fac- too small in another. While in many
tors (usually clutch size). Let us consider cases this may select only for higher
hole-nesting birds, which we discussed intraspecific variation in clutch size, in
earlier. Using this model, we would other cases mechanisms have evolved
expect that hole nesters need to allocate that allow an annual “fine-tuning” of the
less energy to predator avoidance and production of young under such unpre-
thus could put more energy into clutch dictable conditions. These are often
size. Data show that hole nesters have termed bet-hedging strategies. They are
larger clutches than open nesters within adaptive in unstable conditions because
a region, but they also show the same several weeks elapse between the time
latitudinal variation in clutch size, most when a breeding bird lays its clutch and
likely because of changing food supply. the time when it must find enough food
This model can also predict clutch size to feed the offspring. To the extent that
when comparing birds with precocial clutch size is an evolutionarily adapted
young to those having altricial young; “bet” about environmental conditions,
birds with precocial offspring do not these strategies give the bird a chance
face the energetic cost of food gathering to adjust the effective brood size at the
that birds with altricial young face, so we last minute to produce the maximum
might expect the former to have gener- number of viable offspring.
ally larger clutches. In most cases, bet hedging involves
It should be noted that this model what is known as brood reduction.
suggests that larger clutches should Reduction is necessary because it is
appear in populations living in less impossible for a bird to lay a late egg
stable environmental conditions, which when it realizes that conditions will be
would mean that the production of good for raising young. Rather, the bird
young would tend to balance mortality. might initially lay an extra egg and then
This pattern is to be expected because try to come up with some way to quickly
of the varying conditions involved, and dispose of the young bird should condi-
not because the birds are attempting to tions suggest that the brood be reduced.
consciously regulate their populations. This removal should result in a smaller
brood, with the hope that each nestling
Bet-hedging strategies can receive adequate food. In good years,
however, the extra young might receive
Seasonally variable environments also enough food to survive and have good
often show annual unpredictability chances of success.
regarding rainfall, temperature, and so If a clutch hatches with one or two
forth. Anyone who has lived for several too many eggs for resource conditions
years in the temperate zone knows that but with all young of the same size and
one summer season might continue condition, the young all might suffer
chapter 12

for months, while another might occur by dividing the food evenly. The result
for just a few days. Such variability in might be the production of a complete
climate may also affect the evolution of clutch of low-quality young. Species
clutch size, as what may be an optimal that have evolved brood reduction

358

1stPages_B.indd 358 7/22/20 11:54 AM

 mechanisms usually set up a situation which the young have slow growth rates
in which competition within the nest or can store fat, for these attributes
occurs if food is limited and at least one would tend to reduce the intense com-
of the young is at a competitive disad- petition that causes the starvation of a
vantage. In this case, the weakest young young bird.
quickly dies and the brood is reduced. A few species that are exposed to
Such unevenness can be accom- unpredictable, short-term variation in
plished in several ways. Some species lay resources (such as swifts, swiftlets, and
eggs that vary in size, thus resulting in swallows, which are unable to capture
young that vary in size and, presumably, flying insects during rainy weather)
competitive ability. Eggs of the Common have adaptations to help ensure the
Grackle (Quiscalus quiscula) may vary short-term survival of the young. These
in size by as much as 45% of the mean include fat storage and variable growth
egg weight.6 This has been correlated rates, which reduce the effects of days
with potential survival. Some species with little food, and the development of
begin incubation before the clutch is early thermoregulation, which allows
finished. In many raptors, incubation both parents to forage away from the
begins with laying, resulting in young young. Although these techniques are
that hatch at intervals corresponding good for short-term survival, they obvi-
to those at which the eggs were laid. ously work against brood reduction.
Such pronounced inequality may be In most small birds, this intrabrood
especially adaptive in upper-trophic-level competition results in the rapid loss of
carnivores, where food supply may be the weakest nestling. In large species like
variable and high-quality young must be raptors or herons, even the youngest of
produced to have a good chance of sur- the offspring may survive for some time
vival. Many small birds begin incubation before dying. In some cases, it appears
with the penultimate (next to last) egg, that the demise of the youngest bird may
which means that the last egg hatches a not be solely due to lack of food but may
day late. This difference may be enough result from attacks by one or more older
to result in that bird’s starvation if food siblings (called siblicide or fratricide).
Adaptive Variation in Avian Reproduction
is in short supply. In some species, It has been suggested that parent birds
a two- or three-day interval occurs can either encourage or discourage such
between the initiation of incubation and interactions among their young, depend-
the laying of the last egg. ing in part on resource conditions. While
Such mechanisms of brood reduc- some have suggested that siblicide is an
tion would not work for all species. Obvi- aberrant occurrence reflecting unusual
ously, brood reduction by this means food limitations, the frequency of
would not be particularly advantageous apparent brood reduction mechanisms
for birds with precocial young (although suggests that it really may be an adaptive
it has been suggested that precocial birds way to produce young of acceptable qual-
start incubating before the last egg is laid ity in a variable environment.
to reduce the chances of nest predation
before at least some eggs have hatched).
It also would not work for species in

359

1stPages_B.indd 359 7/22/20 11:54 AM

 The Timing of Breeding time is may vary among species, even
within the same habitat. Much of this
The determination of the optimal time variation is related to variation in food
to breed should be the result of natural abundance, and some of it may reflect
selection, with those individuals that differences in food limitation related to
breed at the best time producing more either feeding the young or ensuring
young that survive to breed themselves the success of the fledglings once they
than individuals breeding at other times. are on their own. In a typical temperate
Maximization of an individual’s fitness woodland, the Great Horned Owl (Bubo
would then be an ultimate determinant virginianus) may lay its eggs in January or
of the breeding season, perhaps exhib- February, which means that the nestlings
ited through some genetically deter- must be fed during very cold periods
mined mechanism related to photope- when food may be scarce, but also that
riod or other predictable stimulus. As the young fledge early in the summer
mentioned earlier, while such external when food is abundant and presumably
stimuli may get a bird into breeding con- easier for inexperienced foragers to cap-
dition at what is evolutionarily the proper ture. The predatory Loggerhead Shrike
time, most species also rely on short- (Lanius ludovicianus) also nests very early,
term stimuli that tell them conditions often by mid-February. Other owls breed
are favorable for breeding. These stimuli somewhat later in the spring, along with
may be related to weather conditions, multibrooded species such as the Ameri-
food supply, the physiological condition can Robin and Mourning Dove (Zenaida
of the female, and so forth. There is con- macroura). Most of the migrants from the
siderable variation among species in the tropics arrive in May and breed in late
interaction between these long-term and May or June, often producing only one
short-term factors that affect breeding brood before leaving for the tropics again
seasons. In most species, readiness for in August. A few species, such as the
breeding is determined by photoperiod, American Goldfinch (Carduelis tristis) and
and short-term factors may affect breed- Blue Grosbeak (Guiraca caerulea), may
ing times by only a few days. In contrast, not breed until midsummer, presumably
some of the seed-eating birds that exhibit because their foods are more abundant at
mutualistic interactions with their food that time. An extreme case in this regard
supply seem to respond almost com- is Eleonora’s Falcon (Falco eleonorae) in
pletely to the proximate stimulus of this the Canary Islands, which breeds in the
food supply. Because of this, species fall, when migrant birds constitute its
such as the Pinyon Jay (Gymnorhinus major food. Harris’s Hawk (Parabuteo
cyanocephalus) and Clark’s Nutcracker unicinctus) in the southwestern United
(Nucifraga columbiana) may breed at States and the tropics is known to breed
almost any time of the year when their in both spring and fall.
food is superabundant. Among temperate zone breeders, it
chapter 12

Although it is generally believed that has been observed that nests are ini-
breeding should occur at the time when tiated early enough in the spring that
the most young will be produced for they are often lost to cold conditions,
long-term survival, what that particular yet breeding may cease early in the

360

1stPages_B.indd 360 7/22/20 11:54 AM

 summer, at a time when the food supply of breeding season occurs in the Greater
may be reaching a peak. Suggestions as Antilles of the West Indies. These islands
to why these patterns occur have come are the winter home for great numbers of
from studies of the House Sparrow small, insect-eating warblers (Parulidae);
(Passer domesticus) in the rather extreme in many habitats, these winter residents
environment of Alberta, Canada.7 These greatly outnumber resident insectivores.
studies found that nests were often Under normal conditions, resident
initiated in April, despite low chances insectivores of the Greater Antilles do
of nesting success, but that nesting not breed until late May or June, the time
stopped in early July, when fledging when these potential competitors are
rates were high. This was explained by absent and spring rains have ended the
the survival of young from various parts January–April dry season. Should these
of the breeding season. Even though rains not occur, the resident species will
parents had a small chance of fledging not breed during May–July, and they
young when nesting in April, any young also will not breed after the winter resi-
that did survive had a very high prob- dents have returned, even though heavy
ability of surviving to breed the next autumn rains may occur. In the Lesser
year. Young that were produced later in Antilles, however, where few winter res-
the spring or early summer, when the idents occur, resident birds show much
probability of fledging success was high, longer breeding seasons, often starting
had little chance of surviving to breed. in March or April and extending through
This appeared to be due to dominance the summer. Whether a similar high
interactions in feeding flocks during density of winter residents affects the
winter. Young from April or May were breeding season of mainland insectivores
dominant over young from June or July, is more difficult to determine, although
which apparently favored the survival of some evidence suggests that this may be
the former over that of the latter. Similar the case.
patterns may be at work in favoring the The vast majority of bird species
early breeding attempts of other species breed annually, but some exceptions
where either dominance interactions or do occur. Many large species, such as
Adaptive Variation in Avian Reproduction
foraging experience may be important in condors and albatrosses, will not breed
affecting winter survival of the young. in a year following a successful breeding
The climatic constraints that are attempt. In most of these cases, young
dominant in determining the breeding are produced only every other year. An
seasons of temperate birds are not as intermediate case between annual and
important to many tropical species, biennial breeding sometimes occurs
especially those in rainforests. Not sur- in the Magnificent Frigatebird (Fregata
prisingly, studies have suggested longer magnificens). In this species it takes
breeding periods among tropical birds. about 13 months to fledge an offspring.
Nevertheless, many tropical habitats are Although monogamous through most of
seasonal because of rainfall fluctuations, the nesting period, the male frigatebird
such that breeding occurs during times may desert its mate when the young is
when resources are most favorable. about a year old. At this time, the male
A special case regarding the control then mates with a different female, while

361

1stPages_B.indd 361 7/22/20 11:54 AM

 the previous female remains with the off- must remember that natural selection
spring and fails to reproduce in that year. operates on individuals, not pairs, so
A few species live in environments monogamy must be in the best interests
where either no environmental cues of both the male and the female for both
affect the breeding season or these cues to remain together. Should either sex
occur in something less than one-year have an opportunity to increase its fit-
cycles. The Sooty Tern (Onychoprion fus- ness by behavior other than monogamy,
catus) on Ascension Island breeds with this behavior should be selected for.
about a 9- to 10-month periodicity.8 In That monogamy is necessary for
many tropical seabirds, breeding sea- successful reproduction in many species
sons are not highly synchronized, such has been shown in a variety of ways.
that members of a species may breed Loss or removal of one of the parents
over long, overlapping periods. The use almost always results in loss of some or
of predator-free nest sites would favor all of the young, or in loss of weight in
this spread in reproductive effort, as the young. Either of these outcomes low-
would the competition for food around ers the potential fitness of both parents.
colony sites. Given that both parents have invested
In addition to variation in the length time and energy in pairing and prelim-
of the breeding season along the tem- inary nesting activities, desertion of a
perate-tropical gradient, there is also mate should occur only if it is adaptive.
variation in breeding times associated To measure this, we must know the
with changes in longitude from the effect of this desertion on the number
coast to the interior of a continent, as of young the remaining parent might
well as with altitude and with patterns of produce and the chances the deserting
temperature or rainfall. In many ways, parent has of successfully finding a new
these patterns of climatic predictability mate with which a second breeding
affect the evolution of the breeding sea- could be accomplished. In most cases,
son in much the same way as they affect the survivorship of nestlings with only
clutch size (see above), with stable and/​ one parent or the chances of finding
or more moderate conditions allowing second mates must be too low to select
longer breeding seasons. against monogamous mating systems.
Situations do exist, however, in
Mating Systems which one parent can successfully raise
the young, thereby allowing the other
Sexual reproduction requires the inter- parent to attempt to mate with other
action of a male and female, but mini- individuals. These conditions, described
mally only for the few seconds required by Stephen Emlen and Lewis Oring
for successful copulation. The fact that (1977) as the environmental potential
over 90% of bird species show social for polygamy (EPP), define conditions in
monogamy, in which a pair-bond lasts which the constraints favoring monog-
chapter 12

for much if not all of the breeding pro- amy break down and a polygamous
cess, suggests strongly that both mem- mating system can result. In almost
bers of the pair are needed for success- all cases, the EPP is related to food,
ful reproduction in most species. We because that is most often the factor that

362

1stPages_B.indd 362 7/22/20 11:54 AM

 limits reproductive success. However, start talking about two different systems:
it can also involve nest sites or display social mating systems, which describe
grounds. Because there are two sexes, the actual pairing and distribution of
EPP occurs in several combinations. birds as they breed; and genetic mat-
Polygyny occurs when one male monop- ing systems, which describe where the
olizes the mating of several females. If various genes are actually being distrib-
one female mates with several males, it uted. Of course, it is not evolutionarily
is polyandry. Multiple mates may occur adaptive to raise young that are not your
at once, which results in simultaneous own, so a variety of new conflicts arose
polygyny or polyandry, or they may within these social systems that needed
occur in succession, which results in to be explained. The reality, though, was
serial or sequential polygyny or polyan- that social monogamy was rarely genetic
dry. A variety of other combinations are monogamy, as extra-pair eggs or young
possible if mating behavior is examined were common in the nests of socially
over a longer period. monogamous species.
Because in producing eggs the In most cases, these EPCs and EPFs
female invests much more energy in seem to be a way for individual breed-
reproduction than the male, it is gen- ing birds to try to increase their fitness
erally less adaptive for the male to take within the constraints of keeping their
care of a female’s eggs than it is for a mate, who is still needed to successfully
male to attract multiple females. There- raise young. The general advantage
fore, polygyny is the dominant nonmo- seems to favor older, dominant birds
nogamous mating system, while poly- over younger, subordinate birds in
andry is quite rare. Before we look at the all these interactions. In many cases,
evolution of polygyny, it must be pointed dominant males that have already mated
out that not all monogamous matings with a female search for other females
are as clean-cut as they might seem. with which to copulate, while maintain-
Behavioral work during the 1980s ing a pair-bond with the initial mate
showed the regular occurrence of what (who may not want any extra-pair young
are called extra-pair copulations (known because she is mated to a dominant
Adaptive Variation in Avian Reproduction
as EPCs, or sometimes EBCs for extra- male). Sometimes females from territo-
bond copulations) within what are ries next to the dominant male but with
basically socially monogamous species. male mates who are younger and less
Because birds have such quick copula- dominant will go to the dominant male
tions in most cases, these were hard to to seek copulations. The result is genetic
observe in most species, and in most polygyny in what is a socially monoga-
cases, we did not have any clue as to mous system.
whether these EPCs resulted in extra- Numerous studies of maternity and
pair fertilizations (EPFs). Only with the paternity within socially monogamous
development of a variety of molecular species have shown confusing patterns
genetic techniques in the 1990s could of parentage.9 Attempts to label such
we start to measure actual maternity systems have come up with somewhat
and paternity within clutches. Such tests confusing names. There are some cases
of parentage required ornithologists to of true promiscuity, where mixed mating

363

1stPages_B.indd 363 7/22/20 11:54 AM

 occurs outside the normal social monog- natural selection should favor behaviors
amy. What was called “frank polygyny” that prevent or reduce the number of
involved some males with multiple such EPFs. This might be done by mate
female social mates. “Cryptic polygyny” guarding during critical fertile periods,
was used to label systems that appeared or by high frequencies of copulation
to be monogamous but actually had lots within these pairs composed of a female
of EPCs. Some version of polyandry and a subordinate male, as he attempts
had to be applied to those cases where to swamp the sperm of his dominant
females mated with multiple males rivals. Some of the largest testes and
while males mated with single mates. most frequent rates of copulation ever
“True monogamy” was used to describe recorded occur in monogamous birds
those systems where socially monog- with lots of EPCs, where subordinate
amous species were also genetically males attempt to ensure some paternity
monogamous. within their mate’s nest by high fre-
The occurrence of extra-pair young quency of sex.11 While we might think
(EPY) in bird species is highly vari- that a smart subordinate male would not
able. Species such as the Black-capped put his territory near that of a dominant
Chickadee (Poecile atricapillus) and Tree male, it is possible that he might not
Swallow (Tachycineta bicolor) have rates attract any females to an isolated terri-
as high as 37% and 47% EPY, respec- tory. In addition, by setting up a territory
tively. Such high rates may be related to next to a dominant male, the subordi-
these species being cavity nesters with nate male establishes site dominance,
relatively large clutches, but that has not and he may move up in the dominance
been fully explained. In most species, order in subsequent years, such that he
rates of EPY are in the 10%–20% range. pays a price for all the EPCs in the first
Low rates of extra-pair young (0%–1%) years of his life but compensates for that
occur in most shorebirds, seabirds, and later in life, when he is the dominant
raptors. Rates of EPY can vary season- male with young in multiple nests.
ally. For example, Eastern Phoebes Until recently, models of the evo-
(Sayornis phoebe) have only about 2% lution of avian mating systems were
EPY with first broods but may show forced to rely on information from
up to 24% with second broods. This social interactions between the sexes.
may be because first broods are highly These were nice and clear, though,
synchronous, so pairs stay together because we could see that nearly all
early in the breeding season, while later monogamous species really needed both
broods are asynchronous, which allows parents in order to be successful. Now
birds to explore extra-pair matings later that we can see that social monogamy
in the breeding season.10 The reality is is not necessarily genetic monogamy,
that many to most pairs that are socially we must recognize that the step from
monogamous are also genetically genetic monogamy to genetic polygyny
chapter 12

monogamous. can occur within the mating system of

Obviously, a male whose mate is monogamy, although this is constrained
copulating with other males may end up somewhat because pairs are needed to
caring for young he has not fathered, so ensure production of young, such that

364

1stPages_B.indd 364 7/22/20 11:54 AM

 even dominant males do not produce territory quality, an arriving female may
high numbers of young, as we will see reach a point where choosing a male
is possible in some of the nonmonoga- on a low-quality territory provides little
mous systems. or no chance for success. On the other
hand, if she could mate with one of the
The evolution of polygyny males holding the best territories, she
might actually be able to raise more
Most models explaining the evolution young by herself than she could with a
of polygyny begin with monogamous, male mate on a low-quality territory.
territorial birds, primarily because this The point where a female would
seems to be the dominant, ancestral have greater fitness by raising young by
system in birds. Some special resource herself on a high-quality territory than
condition or behavioral trait that serves by being monogamous on a low-quality
as the environmental potential for polyg-
amy (EPP) is then added, which results
in two distinct shifts in behavior. First, it
allows a single male to mate with several
females (which we have seen can occur
to a limited extent in monogamy), and
most importantly, it frees the female
from requiring care from the male.
The classic model for the evolution
of polygyny is known as the polygyny
threshold model and was developed by
Gordon Orians, Jared Verner, and Mary
Willson in the 1960s.12 They worked
primarily with the Red-winged Black-
bird (Agelaius phoeniceus), which has
become to mating system studies what
the Great Tit is to foraging studies. To
Adaptive Variation in Avian Reproduction
visualize their model, consider a group
of monogamous territorial pairs living
in an environment that is not uniform.
Some of the males are able to defend
territories that are very rich in resources,
while other males defend poor-qual-
ity territories (fig. 12.6). As females
arrive at the breeding grounds, the first
female should recognize the best-quality
territory and attempt to mate with the
male in that territory. The second female
Fig. 12.6. Schematic diagram suggesting how
should mate with the male in the sec-
resource patchiness affects the environmental
ond-best territory, and so forth. At some potential for polygamy (EPP). Circles define
point along this gradient of diminishing territories while dots represent resources.

365

1stPages_B.indd 365 7/22/20 11:54 AM

 territory is termed the polygyny thresh- many vertical feet apparently means that
old.13 For polygynous behavior to evolve the female cannot forage fast enough
from monogamy, behavioral shifts need to raise young by herself, and hence the
to occur such that males can mate with EPP is not present.
multiple females and these females The above form of polygyny is
allow other females to live on their known as resource defense polygyny
mate’s territory. Because males have because it revolves around a male
already invested much energy in gaining defending a resource with which he
the best-quality territories, the adaptive can attract multiple females (fig. 12.7).
value of polygyny is easy to see for them, Resource defense polygyny also occurs
as a male can potentially increase his in some colonial breeders, in which
reproductive success by several times dominant males may control multiple
without greatly increasing his effort. nests or nest sites and are thus able
Even if a male would get only a single to mate with multiple females. Most
additional young from a second female colonial species are monogamous,
mate, it would be adaptive for him. For however, presumably because either the
polygyny to evolve, the behaviors that male serves an important role in the
reduce aggression between females so reproductive effort or the synchrony that
that they can subdivide territories must is advantageous in colonial breeders
result in as many young as females results in few unmated females during
would have if they paired with a male the peak reproductive period. In a few
on a lower-quality territory. Because species, a male is able to defend two
all females within these high-quality separate territories and thereby mate
territories produce young successfully, with two different females. For some
the evolution of these behavioral shifts unknown reason, nearly all of the latter
appears to occur rapidly. cases of polygyny have been recorded
This model for the evolution of in European species, such as the Pied
polygyny requires, at least initially, a Flycatcher (Ficedula hypoleuca).14
gradient in territory quality, with the Other EPPs exist that lead to other
best territories rich enough that a single forms of polygyny (fig. 12.7). In birds
female can successfully raise young. with precocial young, it is not necessary
While this seems simple enough, it does for the adults to bring food to the young,
not occur very often. Most of the polyg- and this might serve to make reaching
ynous species occur in marshes, grass- an EPP easier. Indeed, species with
lands, or early second-growth vegetation. precocial young show higher rates of
These are all very productive habitats, polygyny. Monogamy still occurs, how-
and they are structurally very simple. ever, in cases where both parents may
Food is concentrated in just a few feet be needed to watch for predators, when
of vegetation or, in the case of marshes, the male may be needed to defend a
at the water’s surface. This makes it territory for its mate and young, or when
chapter 12

easier for the female to forage effec- both are needed to ensure adequate
tively. Although mature forests or other incubation of the eggs. The latter case
habitats may be as productive overall, is particularly important among species
the dispersal of this productivity over nesting in the Far North, such as water-

366

1stPages_B.indd 366 7/22/20 11:54 AM

 fowl and sandpipers. In many geese that
Fig. 12.7. Broad-scale model to help understand
Adaptive Variation in Avian Reproduction
the evolution of mating and cooperative are monogamous for life, the female
breeding systems in all birds based on the lays the eggs and then feeds for several
concept of EPP. Mating systems to the right days while the male incubates. Once the
of monogamy are characterized by rich female has recovered from the energetic
resources that allow for reduced parental care stress of laying the clutch, both birds
(fewer than two parents caring for young) and
alternate in incubation, which keeps
pronounced sexual selection. The cooperative
the eggs warm while allowing both to
breeding systems to the left are characterized
by limited space and extended families. See
feed. If there were only a single parent,
text for a full explanation. either that bird would starve or the eggs
would chill and not develop properly
or would die. Both birds stay with the
young throughout development. In
contrast, most temperate or Arctic ducks
are monogamous through the egg-laying

367

1stPages_B.indd 367 7/22/20 11:54 AM

 period, presumably because the male of ularly in fairly complex habitats where
the pair is needed for fertilization of the males are somewhat protected from
eggs or he needs to ensure his paternity predators, the males may be scattered
of the young, and perhaps to defend a throughout the area. In these cases, a
bit of territory for the female and young. female must wander about, evaluating
In most ducks, however, once the clutch males until she makes a choice. In many
is laid the male leaves the breeding cases, however, males congregate in
grounds and the female provides all the display groups known as leks. Leks may
parental care. In contrast, tropical duck occur for several reasons. When display-
species tend to mate for life and both ing, many males adopt either conspic-
parents provide parental care.15 uous colors or behaviors (see below),
For many species of birds with which makes them more susceptible
precocial young, the above constraints to predation, particularly when these
do not occur and polygyny develops. In displays occur in open environments. By
some cases this may be resource defense displaying in groups, these males have
polygyny, in which males defending more eyes to spot predators, much as
the most resource-rich areas mate with foraging flocks do. Grouping may also
the most females (also termed territo- occur to attract females, with the idea
rial harem polygyny). In many cases, that a female who is going to choose
however, because of the independence among a group of males would be
of the female and the young, any terri- more likely to be attracted by an already
torial constraints associated with this assembled group than to wander about
mating system break down. In such evaluating males singly. This would
cases, it would be optimal for a female allow the female the chance to judge
to mate with the highest-quality male males while they were together and
available and then move to the best to see the dominance hierarchies that
nesting habitat available. Each male male-male interactions had developed.
would have the chance to mate with as While the adaptive advantage for one of
many females as possible (rather than the dominant males in a group seems
the maximum number he could fit on obvious, it is less understandable why a
his territory). The result here is termed subordinate bird would remain in a lek.
male dominance polygyny, because the The explanation seems to revolve around
most dominant males usually mate with the ability of larger leks to attract more
the most females. Some have termed females, such that the long-term chance
such a system promiscuity because the of success for a subordinate male may
interaction between male and female be better in a larger lek, but only over the
is so brief, but studies have shown that course of years.
females are doing a great deal of selec- In most leks, males defend tiny
tion regarding male characteristics, such display territories. Following the system
that the laxity implied by promiscuity is used earlier, these may be considered
chapter 12

not present. Type D territories. Generally, the most

Species with male dominance dominant birds have territories within
­polygyny can be arranged spatially in a the center of the lek, with subordinate
variety of ways. In some cases, partic- birds on the periphery. Females usually

368

1stPages_B.indd 368 7/22/20 11:54 AM

 Fig. 12.8. Proportions of total copulations short period. While this is obviously a
accomplished by males in order of polygynous system for the male, who
dominance rank in the Greater Sage-Grouse generally raises only one brood a year, it
(Centrocercus urophasianus) and the White- is a polyandrous system for the females,
bearded Manakin (Manacus manacus). Note who move from male to male through
how a few males dominate copulations in the summer.
these species (Wiley 1973; Lill 1974).
In the various polygynous systems,
each individual should adopt a strategy
choose the dominants; often a few of the appropriate for its social status and
males in a lek participate in nearly all resource conditions. In general, all
the copulations (fig. 12.8).16 Young males females in male dominance polygyny
seem to work their way toward the mid- will get the chance to mate with dom-
dle of the lek with age. inant males and then go off and raise
In a few large species with preco- the young by themselves. In resource
Adaptive Variation in Avian Reproduction
cial young, females move around in defense polygyny, a female must evalu-
small groups that develop relationships ate options depending on the number
with a breeding male. All the females of females mated with a dominant
mate with the male and lay eggs for male and the quality of the territory of
him over a short period of time. This an unmated male. As more females
female defense polygyny results in a mate with the dominant male, a newly
male getting a large clutch of eggs in a arriving female may be better off in
short period; the male then incubates a poorer-quality territory than in an
and raises these young, while the flock overcrowded polygynous territory. Male
of females moves on to another male. strategies may also vary, particularly with
This system results in a male having age and dominance status. In resource
many young that he has fathered, with defense systems, many young males do
a shortened exposure time for the nest not even defend territories, as they can
because multiple females laid over a acquire only poor territories with little

369

1stPages_B.indd 369 7/22/20 11:54 AM

 chance of attracting females. The best mous birds might favor brightly colored
strategy seems to be to wait a year before signals or unusual displays as a part of
even trying (often keeping a female-like intrasexual interactions. The intensity of
plumage in the meantime). In male selection for these markers or displays is
dominance systems, young males may limited, however, by the amount of male
join a lek to establish a position in the parental care, as such markers might be
dominance order. This decision, though, maladaptive if they attracted predators to
should depend on the advantages of the nest when the male is helping out.
joining a large lek (which may attract With the crossing of the polygyny
more females) versus the disadvantages threshold, male-male competition
(it may take longer to become dominant). becomes more pronounced because of
In some cases, a better option might be the greater possible rewards of such
to join a smaller lek that may be visited competition, and also because the
by fewer females but where breeding male role at the nest is often reduced
status may be attained earlier in life. or absent. In a resource defense polyg-
Male dominance polygyny is not ynous system, a dominant male may
confined solely to birds with precocial be able to increase his fitness many
young. Some tropical frugivores are times over that of a subordinate male.
involved in mutualistic interactions with If extravagant colors or displays aid in
fruits that are more nutritious than most achieving this dominance, they will be
fruits. In these cases, the female may be quickly passed on to the dominant bird’s
able to collect enough food to feed the many offspring. Among male domi-
young, which serves as an EPP; these nance polygynous systems, a dominant
species also have the small clutch typical bird may be able to achieve an almost
of tropical birds. Among the New World unlimited number of matings, which
species with male dominance polyg- further selects for any advantageous
yny are manakins and cotingas, while colors or displays. With the reduction
the Old World is known for its birds of of nest-related behaviors acting as a
paradise and bowerbirds. Whereas these control on the expression of these sexual
New World forms are generally small, traits, the sky almost becomes the limit.
the Old World forms are large, perhaps Predation tends to serve as the chief
because they are able to use large foods factor limiting sexual dimorphism,
made available by the absence of mon- although in many cases this does not
keys in Australia and New Guinea. Most seem to have had much effect. Among
nectarivores, such as hummingbirds the birds of paradise, incredibly bizarre
and sunbirds, are polygynous, presum- plumages and behavior occur, including
ably because of the fairly easy availability some males that hang upside down and
of high-quality food in the flowers on show their brightly colored bellies. Some
which they feed.17 of the New World manakins combine
bright colors with group displays, where
chapter 12

Sexual selection in polygynous systems two or three males move in synchrony

to attract a female. When examining
In chapter 11 it was pointed out how a bird book, we can safely predict that
male-male competition among monoga- those species with really bizarre male

370

1stPages_B.indd 370 7/22/20 11:54 AM

 plumages or mating rituals are most these cases, it appears that the bower
likely polygynous. The greater the dif- has taken over the role of gaudy plum-
ference between male and female, the age as a signal of male quality. This still
more likely it is that a nonmonogamous allows females to evaluate and choose
mating system is involved. Because among the males, but it reduces preda-
male-male competition often involves tion rates on the males when they are
fighting, polygynous males are also not involved in sexual displays. Recent
often much larger than the females with work with some of these bowerbirds has
which they mate. shown that different populations seem
The costs of such gaudy plumages to favor displays dominated by different
are paid in higher predation rates. Many colors, perhaps as a result of cultural
open-country species with polygynous preferences. These preferences were
systems, such as prairie grouse, cannot tested with some ingenious experiments
afford to be bright red all the time, so by Jared Diamond (1982), who used
they trade bright colors in the feathers colored poker chips as an experimen-
for brightly colored, inflatable air sacs tal tool. In addition to discovering the
and spectacular display dances. In this birds’ color preferences, he also found
way, when they go off to feed they can that male bowerbirds spend a lot of
look like a typical cryptic grassland bird, time stealing colored objects from one
yet when they are competing for females ­another’s bowers.
they can be quite attractive. Forest birds Because young males often do not
are apparently somewhat less vulnerable have enough status to achieve success-
to intensive predation pressure, as they ful matings in polygynous systems,
more often have bright colors. in many cases they also avoid paying
An interesting compromise between the costs of the male plumage by not
the strong selective pressures favor- acquiring it until later in life. This is
ing sexual displays among males and known as delayed maturation, and it
the costs of predation when males are occurs in many polygynous species. In
brightly colored may have been struck some cases, young males may use their
in some bowerbirds. These tropical female-like appearance to sneak in occa-
Adaptive Variation in Avian Reproduction
frugivores of Australia and New Guinea sional copulations while they are visit-
include many species with male domi- ing male territories. Because they look
nance polygyny. Some species have the like females, territorial males may not
more typical polygynous situation, with exclude them, giving them the chance to
ornately colored males that display to mate. These sneaky strategies are gener-
attract females. Some of these modify ally considered secondary strategies that
their display locations by building struc- develop after the adaptations associated
tures known as bowers, which aid in the with the primary strategy (for example,
displays. a male evolves a female-like appearance
Other bowerbirds are quite dull col- because of the pressures of polygyny and
ored (at least to the human eye), but they is then able to evolve behaviors that aid
build extravagant bowers that are highly it in sneaking copulations).
decorated with colored leaves, fruits, or Perhaps the most striking sneaky
any other colored material available. In strategy occurs in the Ruff (Philoma-

371

1stPages_B.indd 371 7/22/20 11:54 AM

 chus pugnax), a European shorebird always fairly cold, the breeding season
known for the individual variation in the is short, and it is far from the wintering
colored plumage of the display collars grounds. Most sandpipers are monog-
of dominant males. The difference amous, pairing during migration or on
between sexes is so striking that the the breeding grounds. After this pairing
female has its own common name, the occurs, the female lays a clutch of three
Reeve. These colored Ruff males defend or four relatively large eggs. At this point
small territories within leks, as do her energy reserves have been depleted,
most lekking species, but for years we both from the long migration and from
have known that Ruff males with white egg laying. This depletion is accentuated
collars also exist. These white-collared by the small size of shorebirds, which
Ruffs behave subordinately to the col- limits the amount of energy they can
ored Ruffs, which allows them to remain bring with them. (In contrast, many
on colored Ruff territories. When a large waterfowl are known to accumu-
female arrives at a lek, the colored Ruffs late energy reserves on the wintering
are sometimes so busy displaying and grounds that can be carried to the
defending their territories that the white breeding grounds to provide energy for
Ruff male is able to copulate with the egg production.) Because the female
female. In 2009, scientists also dis- sandpiper needs to feed heavily, when
covered that some male Ruffs adopt a she finishes laying, the male begins
female plumage, which also allows them almost continuous incubation of the
to sneak in copulations while the color- clutch. Generally, he will incubate by
ful males fight.18 himself for several days, until the female
has replenished her reserves and can
Avian polyandry take her turn with incubation while her
mate feeds. Because of these energetic
The tremendous investment of the constraints, and perhaps also because of
female in the production of eggs usually the need to keep a pair together in case
means that it is the female who has the the clutch needs to be replaced because
most to lose by leaving a monogamous of predation, in most shorebirds the
pair. As a result, polygyny is the domi- pair remains together throughout the
nant nonmonogamous mating system. remainder of the breeding process.
Only two to three dozen species of birds This system results in two behaviors
in the world show mating systems that that serve as preadaptations for polyan-
can be classified as polyandry. Most of dry. First, males develop a strong attach-
these species are among the sandpipers ment to a clutch of eggs, with a large
and have evolved this behavior because amount of time and energy invested
of traits peculiar to this group and their in the clutch during the egg-laying and
northern nesting habitats. early incubation periods. On the other
Most of the sandpipers (Scolopaci- hand, females are selected for an abil-
chapter 12

dae) breed in the High Arctic, where the ity to lay a set of eggs and then rapidly
tundra provides many readily accessible recover the necessary energy reserves
insects for their precocial young. This to lay a replacement set, should that
habitat has disadvantages in that it is be necessary. Because of the male’s

372

1stPages_B.indd 372 7/22/20 11:54 AM

 commitment to incubation, the female
does much foraging on her own during
this period. Given these behavioral
adaptations, the proper environmen-
tal conditions are all that is needed to
serve as an EPP favoring polyandry. Not
surprisingly, the EPP can be provided
by unusually rich resource levels, which
often occur in the Arctic because of early
warm weather that increases the num-
ber of insects.
With the behavioral system outlined
above and extremely rich resource condi-
tions, several options are available to the
female. After pairing and laying the first
clutch, she may be able to replenish her
energy reserves rapidly enough to lay a
second clutch. Because food is plentiful,
both parents can incubate a clutch and
find enough food to survive during brief
forays away from the nest. This “double
clutching” doubles the reproductive
potential of both sexes but retains a
monogamous system.19
Once females have adapted to laying
clutches in fairly rapid succession, the
presence of nonpaired males may lead
Fig. 12.9. Distribution of number of male
to a breakup of the monogamous pair-
mates in two polyandrous species, the Spotted
bond. All that then must occur is that Sandpiper (Tringa macularia) (top) and the
a female ready to lay a second clutch American Jacana (Jacana spinosa) (bottom). Adaptive Variation in Avian Reproduction
be courted by an unmated male with a Note how this success compares to that of
territory. selected males shown in figure 12.8.
Under these circumstances, she can
lay a clutch for this mate and then per-
haps lay yet another for herself, or just only one female during a breeding sea-
have time to recover from the energetic son (fig. 12.9). Because the sex ratios for
investment. In this manner she can most species are usually approximately
double or triple her reproductive output, even, we might question whether extra,
while the male does not desert the eggs nonmated males actually occur. They
because of his accumulated investment may exist as a result of nest predation
in them. The result is what is known rates; if clutches are lost to predation
as sequential or serial polyandry, where faster than females can replace them,
a female may lay eggs for a series of then females ready to lay may outnum-
males, while each male may mate with ber males with territories but no mates.

373

1stPages_B.indd 373 7/22/20 11:55 AM

 As a result, males must compete for such as the Spotted Sandpiper (Actitis
these limited females. Thus, even if macularia) that are sequentially poly-
equal numbers of males and females androus in the northern parts of their
occupy the breeding grounds, the num- breeding range may show simultaneous
ber of females capable of breeding at a polyandry in the more southern parts.
given moment may outnumber the terri- In the tropical marsh-dwelling jacanas,
torial males, thereby driving the poly- this system is generally more stable,
androus system. (The sex ratio of birds although migratory jacanas near their
actually able to breed is often defined as northern breeding limits may show
the operational sex ratio.) sequential polyandry.
In a few species of shorebirds that If the males in a simultaneously
nest in more southerly regions, a more polyandrous group receive their clutches
confusing set of behaviors seems to from the female in succession, during
result from these interactions. In these which time each male monopolizes
cases, a male may attract a female and copulations with the female, the system
get her to lay a set of eggs, but he will is genetically very similar to sequential
then try to mate with other females polyandry.21 There is evidence from the
and get them to incubate the second jacanas, however, that a female copu-
clutches. He may then return to take lates with several of the males within
care of the first clutch. As a result, some her territory on the same day and lays
males may mate with more than one eggs in the nests of different males on
female, and some females may lay for subsequent days. In this case, a male
more than one male, a system known as may be raising a set of young with
rapid multiple clutch polygamy.20 mixed paternity, although whether a
In a few species of shorebirds and particular male gains or loses by such a
the tropical jacanas, a slightly different system depends on his overall participa-
system occurs where females defend a tion in copulations. If all males copulate
territory and several males subdivide with the same frequency, each nest
this territory and maintain continual contains a similar mix of eggs in terms
pair-bonds with the female. This is of paternity. Given that jacana nests
known as simultaneous polyandry. It seem to be subject to high predation
seems to have evolved from sequential rates, this mixing of paternity among
polyandry in areas (such as southerly nests may be a safer strategy for a male
temperate breeding areas) where the jacana, as the chances that at least a few
breeding season is long enough and/​ of his offspring survive from one of the
or the predation rates high enough that nests may be higher than the chances
there are advantages in a female main- that a nest with all his offspring might
taining some interaction with a male succeed. The fact that these polyandrous
for which she has laid eggs. This may systems involve a nest for each male-fe-
be achieved through territorial behavior male bond, even though the eggs may
chapter 12

and presumably increases the female’s have mixed paternity, distinguishes

chances of laying any replacement them from other forms of polyandry to
clutches needed while also reducing be discussed below.
the time needed for pairing. Shorebirds The changes in the reproductive

374

1stPages_B.indd 374 7/22/20 11:55 AM

 roles of males and females that occur from monogamy to polygyny on one
in polyandrous systems such as those hand, and to sequential or simultane-
outlined above also affect patterns of ous polyandry on the other.23 Whereas
sexual dimorphism. Not surprisingly, polygamous mating systems seem to be
polyandrous females are often larger connected either to habitats with predict-
than males, presumably because ably rich resource conditions or to spe-
they can be more efficient egg-laying cies that move about in search of these
machines when larger, but also because conditions, more work will be required
size may be important in female-fe- to understand why some species have
male contests for males. In some cases, evolved toward polygyny while others
these female-female interactions or developed polyandry.
female roles in attracting males result in
females that are brightly colored, while Group Breeding Systems
males, relegated to incubation and other
normally maternal duties, are dull col- The mating systems described above
ored. While the egg-laying duties of the include about 97% of the bird species
female seem to work against the devel- of the world. In those systems, care of
opment of bright coloration in most the eggs and young is provided by the
species, in the phalaropes (Phalaropo- father, the mother, or both (ignoring any
didae), painted snipes (Rostratulidae), extra-pair fertilizations). Nearly all of
and a few other species, a phenomenon the remaining 3% of bird species have
known as reverse sexual dimorphism reproductive systems in which a clutch
occurs (although the term in some ways of eggs is cared for by a group of birds
makes no sense). In these, the female that numbers more than two; these
is brightly colored and the male dull, groups may consist of either multiple
although all phalaropes are not known male or female potential parents, or
to be polyandrous. It is not surprising birds that are not active breeders but
that female plumages may be somewhat that serve as nest helpers. Although
more limited in polyandry than those of cooperative breeding has often been
males in polygyny if we again consider examined separately from mating sys-
Adaptive Variation in Avian Reproduction
the relative reproductive costs of males tems, it can be argued that the choice of
and females. Even polyandrous females not breeding and staying to help other
are limited to just a few males by the breeders is at least as extreme a decision
number of eggs they can lay (fig. 12.9); as sharing a mate or giving up paren-
they can never reach the reproductive tal care. We can define the cooperative
potential attained by some polygynous mating system as one with an associated
males, as noted above.22 This should group of breeders and helpers that coop-
then limit the expression of colorful erate in raising young, although not all
female plumages and may explain why individuals are genetically involved (fig.
many polyandrous shorebirds do not 12.10). As with the polygynous systems,
show any sexual dimorphism at all. the formation of these breeding systems
The shorebirds are an interesting is driven by EPPs, but in these cases the
group for the study of mating systems EPPs are associated with limitation of
because they show the range of variation space and/​or food, such that subordinate

375

1stPages_B.indd 375 7/22/20 11:55 AM

 birds are forced to join groups to stay it).24 More commonly, this cooperative
alive and must “make the best of a bad monogamy includes a monogamous
situation.” breeding pair and a group of nonbreed-
These often rather complex breed- ing helpers in what are known as help-
ing systems are classified as communal ing or cooperative breeding systems.
or cooperative breeding systems, but In many cases, studies have shown that
they may include cooperative polygyny these cooperatively monogamous spe-
(where one male and several females cies are also genetically monogamous, in
share a nest and all have genetic part because the group is composed of
investments in at least some of the related individuals where extra-pair mat-
eggs), cooperative polyandry (where ings would involve kin. We will divide
one female and several males share a our discussion of these group breeders
nest but all the males have a chance of into two categories, one comprising a
fertilizing the female), or some form of few species that breed in groups that are
cooperative monogamy. In a few species rather temporary and not confined to
such as anis (Crotophaga), this coop- territories, and the other representing
erative monogamy involves groups of the majority of group breeders, in which
monogamous pairs that share the same groups are often long term, attached to
nest (although they also often compete territories, and highly cooperative.
in trying to contribute the most eggs to
Nonterritorial group breeders

Nonterritorial group breeding occurs in

several forms among the ratites and tina-
mous. In some cases, groups consisting
of one male and several females form,
with all the females contributing eggs to
a nest over several days. At this time, the
system is a form of polygyny, but once
the clutch is complete, the females move
on to mate with another male while the
male incubates the eggs and raises the
young. This development represents ter-
ritorial harem polygyny for the male but
sequential polyandry for the female, a
system common in rheas and tinamous.
In contrast, an ostrich male mates
with a dominant (major) female who
initiates egg laying and stays with the
Fig. 12.10. Relationship between nesting success male throughout the nesting cycle. After
chapter 12

and group size in the Green Woodhoopoe the major female begins laying, other
(Phoeniculus purpureus). Note that groups females also contribute to the nest.
produce more young than pairs do (Ligon and Because too many eggs are laid for the
Ligon 1978). pair to incubate, many are rolled away

376

1stPages_B.indd 376 7/22/20 11:55 AM

 by the major female. She apparently can ute. Acorn Woodpeckers (Melanerpes
identify her own eggs, thereby reduc- formicivorus) seem to be limited by the
ing potential losses to her own and her larder trees that they make and maintain
mate’s fitness. The possible selective (chapter 8),25 while Green Woodhoopoes
advantage to the breeding pair for the (Phoeniculus purpureus) are apparently
presence of these extra eggs may lie in limited by roosting cavities.26 In some
the satiation of nest predators, which species it appears that the amount of
can usually eat only a few of the giant territorial space may not be as important
ostrich eggs with each attack. The as the availability of marginal habitats
secondary females apparently lay the in which nonbreeding birds can survive
eggs despite their low chance of success when breeding territories are full. The
because they constitute the only possi- structure of the habitat may also be
bility of breeding for low-dominance, important, as birds that can readily hide
probably young, females. within their habitat types may not have
such strong selective pressures toward
Breeding groups on territories joining groups as those living in open
environments (see below).
Breeding groups that maintain territo- Many bird populations are large
ries represent the other option in coop- enough that more potential breeding
erative breeding systems. While this individuals exist than breeding territo-
type includes diverse mating behaviors, ries. Numerous removal experiments
all tend to share a few common charac- in different habitats suggest that large
teristics that result in the maintenance numbers of nonterritorial birds are
of breeding groups. wandering about looking for mates and
Nearly all group-breeding species territories. These are termed “float-
occur in situations where their popula- ers” by some because of their drifting
tions have saturated their environment, behavior, while others refer to them
such that some limiting factor, often as the subterranean component of the
simply territorial space, is hard to find. population because they must sneak
Group-breeding species are more com- around avoiding territorial birds. These
Adaptive Variation in Avian Reproduction
mon in tropical or subtropical habitats, birds are usually younger, less dominant
apparently because these are more likely members of the population. After a year
to contain populations near or even or two of floating, they normally develop
exceeding carrying capacity. Long-lived enough status within the population to
species are also more likely to show be able to acquire a territory and a mate.
group breeding, as are species with low Species that show territory-based
reproductive rates, delayed maturity, and group breeding seem to be distinctive
low dispersal. All of these are traits of because the option of floating until
populations that remain at or very near sufficient dominance is achieved is not
the saturation level of their environment. available to them. For this to be the
While breeding territories seem to case, there must be a lack of marginal
be the most common limiting factor habitats, those unsuitable for breeding
that leads to group formation, more territories, where these birds can live,
specific requirements may also contrib- and it must also be difficult for them to

377

1stPages_B.indd 377 7/22/20 11:55 AM

 sneak around within other birds’ territo- costs of keeping additional individuals
ries. At its simplest, it appears that some on a pair’s breeding territory must be
young birds are faced with the option less than the benefits to the breeding
of dispersing to nonexistent habitats, birds, while the young birds must get
which implies a high risk of mortality, more out of joining a group than they
or staying put, which requires some sort would by living alone. Since most young
of alliance with the existing territory birds join groups in which they do not
holders if the bird is too conspicuous to breed but instead serve as “helpers” to
sneak around within the territory. the breeding pair, they have effectively
This relationship between the lack evolved a strategy of not breeding, at
of marginal habitat and group breed- least for some time. Let us examine how
ing is best exemplified by the classic a breeding pair and its helpers justify
study on group breeding done by Glen this apparent alliance, focusing only
Woolfenden and John Fitzpatrick on the on those species where a monogamous
Florida Scrub-Jay (Aphelocoma coerules- breeding pair is assisted by nonbreeders
cens).27 Florida Scrub-Jays are confined (the classic case of “helpers at the nest,”
to sandy habitats with scrub vegetation or cooperative breeding).
in Florida, where all available habitat For group breeding to be adaptive to
is incorporated within territories. A a monogamous pair with helpers, these
dispersing young jay apparently has only helpers must contribute to the increased
a low chance of success. Instead, group fitness of the breeding pair over their
breeding has evolved. reproductive life spans. If pairs with
Western Scrub-Jays (A. californica) helpers produce fewer young than pairs
are common throughout the western without helpers, the genes favoring
United States, however, where they live acceptance of helpers should rapidly
in a variety of habitats. Young scrub- disappear from the population. How this
jays in this region can live in marginal benefit occurs, though, may vary greatly
habitats until old enough to breed, from species to species.
and breeding groups have never been Because the birds that help are most
recorded. The population of scrub-jays often the offspring of the breeding birds,
on Santa Cruz Island off the coast of Cal- the parents may be increasing their
ifornia also never has breeding groups, own fitness by enhancing the survival
apparently because breeding territories prospects of their helper offspring long
do not occur in all habitat types, so that enough to allow them to establish domi-
juvenile birds have habitats where they nance so that they can acquire territories
can survive until they achieve enough of their own.
dominance to acquire a territory. Second, the helpers may assist in a
Monogamous breeders with helpers. variety of nest-related activities, includ-
While the above conditions are appar- ing territory defense, nest building, nest
ently necessary if it is to be adaptive for defense, feeding the young, and repel-
chapter 12

young birds to remain within breeding ling potential predators from the nest
territories, they are not the only require- and young. The effect of this assistance
ments for the development of some may be to increase the chances of suc-
form of group breeding. Rather, the cess for the parents, and a number of

378

1stPages_B.indd 378 7/22/20 11:55 AM

 studies have shown that breeding groups male helper (often his son) takes over.
fledge more young than breeding pairs Because such a mating could result in
(fig. 12.10).28 Depending on the activities incest, when this occurs the helper’s
in which helpers participate, their benefit mother is replaced by a female from
may occur late in the breeding cycle; outside the family group. Male helpers
studies of some species have suggested also tend to roam throughout the year,
that the presence of helpers resulted in apparently assessing the situation in
higher survivorship of fledglings, even neighboring territories. Should one of
when the fledging success of helper and these territories become vacant, they
nonhelper nests was the same. will attempt to acquire it. Finally, as the
What does a helper get by expend- number of helpers increases the group
ing effort in helping even though it is size, the group may also increase the
not the genetic parent of the young? size of the territory it can defend. In the
First, it remains alive; in most helping Florida Scrub-Jay, this sometimes results
species the environmental constraints in the dominant male eventually taking
are such that a young bird faces a help- over part of the parental territory to
or-die choice. While helping, the bird establish his own territory.
gains experience in a variety of breeding Although nearly all the evidence
activities that may increase its chances shows that helpers do help in some
of nesting successfully if given the manner, individual strategies should be
chance later in life. Because the young expected within this general mold. Work
individuals aided by most helpers are with the scrub-jays suggests that first-
their genetic siblings (brothers and year birds do relatively little helping, pre-
sisters), which means that they share sumably because they have little chance
many genes, the helper may be gaining of acquiring a territory anyway, so it is
fitness through what is known as kin adaptive to just lie low and take it easy.
selection (the increase in an individual’s To avoid matings between parent and
fitness through shared genes of rela- young, one of the sexes must disperse
tives). A great debate has raged over the from the territory. As this is usually
role of kin selection in the evolution of the female, helping systems often have
Adaptive Variation in Avian Reproduction
helping behavior. While its role cannot more male than female helpers. While
be discounted, in many cases it has there are advantages to a bird in helping
been shown that helping would be and its parents, if they already have many
is adaptive even if the helping is done helpers it might be advantageous for a
with unrelated breeding birds. While young bird to help unrelated birds, as in
the helper is performing all the activ- this way the helper would be able to rise
ities described above, it is improving to a more dominant position within at
its status, which means that it is slowly least that territory.
moving itself into position to obtain a The final reward for a bird that serves
territory of its own. a stint as helper is to acquire a territory,
Territory acquisition by dominant breed, and then have helpers of its own.
helpers occurs in several ways. In some This suggests that under such saturated
cases, the death of the male terri- conditions, it is adaptive to trade reduced
tory holder means that the dominant nesting success early in life for a higher

379

1stPages_B.indd 379 7/22/20 11:55 AM

 chance of breeding and attaining high Because females do this only before
reproductive success later in life. The they lay, and older females often lay
bottom line in the evolution of all species later than younger females, a skew in
is lifetime reproductive success (fitness), reproductive success often favors older
but with most species we tend to focus on pairs. In four or five species, breeding
annual production. Species with helpers groups are composed of one female and
at the nest force us to look at lifetime several males that share a single nest.
strategies that are effective under such This is known as cooperative polyandry
severe population constraints. because it involves both polyandry and
There is great variation within coop- helping, depending on who fathers the
erative breeders in terms of the duties young and how many offspring there
the helpers perform. In some species, are. A final special case occurs in the
helpers do everything the parents do but Acorn Woodpecker (Melanerpes formiciv-
mate, while in others they are relegated orus), which breeds in groups associated
only to defense of the nest or territory. with their larder trees (chapter 8). These
An interesting situation that may serve groups consist of a core of breeders plus
as an evolutionary pathway to helping helpers. This core of breeders may be
behavior was found in the Green Jay a monogamous pair, one male and two
(Cyanocorax yncas) in South Texas.29 females (sisters), or two males (brothers)
Here, young birds are allowed to stay and one female. This has been labeled
in the parental territory for over a year, cooperative polygamy or polygynandry.
where they assist in territorial defense It functions in much the same manner
but do not aid with nest-related behav- as typical monogamous cooperative
iors. When a new set of young fledge, breeding systems, although the larder
the year-old young are then chased from trees seem to take the place of territories
the territory. as the limiting environmental factor that
Other group breeding systems. Of the favors group formation. It also differs
3% of bird species that regularly breed from monogamous systems because
in some form of group, most exhibit a member of the breeding group that
monogamy with helpers. In a few is lost to mortality is often replaced by
species, a group of males and females a pair of brothers or sisters, thereby
shares a nest or nests, and promiscu- resulting in these polygamous breeding
ous matings apparently occur. In sev- groups. Although we might expect sib-
eral flocking species, breeding is done lings to be highly cooperative because of
by a group consisting of one or more the kinship factor, competition between
monogamous pairs plus the helpers, females has been observed in the form
who may help at several nests. Anis of egg-throwing behavior.
(Crotophaga) are unusual in that sev- These nonmonogamous
eral monogamous pairs share a single group-breeding systems seem to share
nest.30 All females may lay in the nest the spatial constraints found in monog-
chapter 12

and all help raise the young, but the amous species with helpers. The exis-
actual reproductive success of various tence of unusual mating habits is harder
pairs is sometimes uneven because to explain. In some cases, we simply
the females throw eggs out of the nest. may not understand the breeding rela-

380

1stPages_B.indd 380 7/22/20 11:55 AM

 tionships involved. For example, Harris’s This hawk breeds in groups of usually
Hawks (Parabuteo unicinctus) breed in three or four males, but sometimes up
groups that were formerly considered to eight males and one female share
to be cooperatively polyandrous. Recent a territory and nest; all males copu-
work utilizing electrophoretic paternity late with the female and cooperate in
testing, however, has shown that only raising the young. These groups may
one of the males in the group actually produce more young on average than
mates with the female, so the system monogamous pairs, but on a per male
is monogamy with helpers rather than basis polyandrous males lag far behind
polyandry. Further studies may reveal monogamous males in the production
more examples like this. Harris’s Hawk of young. Further evidence that group
is also unusual because recent work breeding has its limitations comes from
suggests that group foraging for rabbits the observation that once a group forms,
may be a strong factor favoring group no new males are added to it with the
formation, rather than some limitation death of a group member. Rather, the
of habitat. group declines in size until monogamy
Where some form of group-related results.
polygamy does occur, it may be related While this suggests that polyandry is
to both the severity of the constraints not the best option for a male ­Galapagos
resulting in group breeding and the Hawk, it has its rewards. Territorial
relatedness of group members. Among birds survive at a much higher rate
species with cooperative polyandry, the (over 90% annually) than birds off
Galapagos Hawk (Buteo galapagoensis; territories (50% or less). A male that
fig. 12.11) may present the most extreme
set of constraints in both these regards.31

Fig. 12.11. A male Galapagos Hawk (Buteo

galapagoensis; at left) and a female on her
nest (above). This particular female cooperated
with three males who all had a chance to
father young and all provided parental care
(Faaborg, de Vries, Patterson, and Griffin
1980). Photos by John Faaborg.

381

1stPages_B.indd 381 7/22/20 11:55 AM

 can join a group and acquire a territory also breeds regularly in polyandrous
early in life may have to live with lower groups.32 In this case, these groups
annual reproductive success, but the are most often trios composed of two
increased survivorship must more than brothers and a female, where one of the
compensate for this during his lifetime. brothers is usually the dominant breeder
The alternative, if all males are monog- while the other mostly helps. This sys-
amous, is for the average male to wait tem is easier to understand because the
a long time before gaining access to a helping brother receives the benefits of
breeding territory, if he can live long kin selection, and the chances are good
enough. On some of the islands on that he will be able to breed by himself
which this species lives, virtually all the in a subsequent year. Without the bene-
land is incorporated into breeding terri- fits of kinship and with a long life span,
tories, which makes life for nonbreeders Galapagos Hawks apparently cannot
very difficult. afford to only serve as helpers.
Why do male Galapagos Hawks Although it may seem that we have
share equal status in terms of reproduc- covered every possible option available
tion, rather than have a dominant male to birds for mating, this is not the case.
with helpers? It appears that juvenile A variety of other strategies have been
hawks are poor helpers for their parents, recorded. Several gull species regularly
primarily because it may take a long show female-female pairs. These are
time for a hawk to become an efficient apparently able to produce viable young
forager. As a result, young are expelled through copulations with paired males
from natal territories at three to four within the colony. They may occur
months of age. Therefore, it is difficult because of a shortage of males within
for young males to form alliances with large colonies.33
related individuals. If male groups are Among the fairy wrens of Australia,
composed of unrelated individuals, the many of the breeding systems involve
costs to a male of a system that would cases where siblings remain on the
make him the subordinate bird may be parental territory to breed.34 Obviously,
too great for him to simply assist the cooperating brothers and sisters do not
breeding male. In a system with ranked mate because of problems associated
dominance, the subordinate individual with incest, so both sexes copulate
might act as a helper for many years with neighboring birds to try to ensure
until he is the sole surviving male. At genetic variation, but mistakes are
this time, he could breed, but without sometimes made when closely related
the aid of helpers of his own. birds do mate.
These costs would appear to be pro- Most species show at most two
hibitive. Instead, birds will cooperate in mating systems, usually monogamy
territory acquisition and other behavior plus a form of helping or polygamy. The
only if they have an equal chance at cop- Dunnock (Prunella modularis) is unusual
chapter 12

ulating with the female, which appears because of the great variety of mating
to be the case. systems it exhibits.35 This small brown
The Tasmanian Native Hen (Gal- sparrowlike bird of northern Europe is
linula mortierii) is a moorhen that distinctive because individuals of both

382

1stPages_B.indd 382 7/22/20 11:55 AM

 sexes establish personal territories. The ductive strategy generally unavailable
way in which these territories overlap in other animals, one known as brood
greatly affects the type of mating system. parasitism. In this system, one species,
When male and female territories are the parasite, lays its eggs in the nest of
similar in size and location, monogamy another species, the host, which pro-
results. When a male is able to defend vides incubation and parental care to
a territory rich enough in quality that the foster young. In birds with altricial
two or more females can establish their young that require much care, the costs
territories within his, polygyny results. to the host of raising a parasite can be
In cases of low habitat quality, females high (as are the benefits to the parasitic
establish large territories that may offspring). In birds with precocial young
include the territories of two males. In that care for themselves in many ways,
some cases, both these males mate with both the costs and benefits of brood par-
the female, who lays only one clutch of asitism are reduced. This system occurs
eggs. While this looks like cooperative only in birds because in animals that do
polyandry, the males compete in a vari- not provide care for their young (such
ety of ways that suggest an uncoopera- as lizards), such parasitism is of little
tive polyandrous bonding. benefit, while in mammals the close ties
Studies of mating and helping from birth between a mother and her
behavior have provided a great deal of offspring make it nearly impossible for
exciting information on avian repro- another female to sneak her young into
ductive strategies. With the recent use a litter, while the male of is no use in
of molecular techniques to determine suckling a baby.
parentage, we have been better able to A brood parasite gains the possible
define the systems and see the individ- advantages of having its young raised by
ual rewards available to different group other birds, which reduces the energy
members. In addition, many of these required for reproduction, and being
species require long-term studies to able to spread its clutch among a num-
elucidate the actual breeding system ber of nests, which increases the chance
involved. Many studies are underway that at least some young will avoid nest
Adaptive Variation in Avian Reproduction
and should provide much interesting predation and survive. Given the latter
information in the future. factor, it is not surprising that brood
parasitism is most common in tropical
Brood Parasitism regions. Of course, raising parasitic
offspring is not advantageous for the
We have shown that reproduction is host birds, so evolutionary responses
both a lot of work, given the energy have often developed to reduce the fre-
required to manufacture and incubate quency of such parasitism. Additionally,
eggs and to raise young, and a gamble, a parasite cannot put eggs in the nests
since at any moment all this effort may of all species because of differences in
be lost to predation. The presence of an egg size, in the begging behavior of the
egg stage when parent birds are strongly nestlings, and in the diet of the host. It
attracted to relatively inanimate objects appears that the diet of the host must
provides the opportunity for a repro- include insects, as brood parasites that

383

1stPages_B.indd 383 7/22/20 11:55 AM

 lay in the nests of frugivorous birds are of nests in England were parasitized),38
rarely successful. population dynamics are usually not
About 1% of bird species are brood affected. When parasites come into
parasites that collectively parasitize contact with small populations that
a large number of other species. The have not previously encountered para-
largest group of parasites is among the sitism, however, host populations can
cuckoos (Cuculidae), in which about half suffer. Noteworthy examples are the
of 130 species are brood parasites. Nearly Kirtland’s Warbler (Dendroica kirtlandii)
all of the parasitic cuckoos are found of Michigan, which did not have to deal
in the Old World. Five cowbirds (Icteri- with brood parasitism until agricultural
dae) are parasitic, along with the hon- practices resulted in an expansion of
eyguides (Indicatoridae), two genera of the range of the Brown-headed Cowbird
finches from the family Ploceidae, and a (Molothrus ater); and the Yellow-shoul-
duck species. The duck, the finches, and dered Blackbird (Agelaius xanthomus)
one of the cowbirds (see below) do not of Puerto Rico, which has recently had
seem as costly to their hosts as the cuck- to deal with parasitism from the Shiny
oos and most of the cowbirds. For exam- Cowbird (Molothrus bonariensis). Both
ple, the Black-headed Duck (Heteronetta species are now considered threatened,
atricapilla) can raise itself once it has in part because of the effects of cowbird
reached a day or two of age, and thus it parasitism, although other factors have
has little effect on its hosts’ reproductive made them susceptible to this problem.
success.36 There is some evidence that In a few cases, such as the Black-capped
nests of estrildid finches that are parasit- Vireo (Vireo atricapilla) of Texas, massive
ized by viduine finches may raise more cowbird removal appears to have been
total young because of the stimulus successful in saving the species, at least
provided by the viduines.37 Cuckoos and for the time being.39
cowbirds are generally more detrimental Of course, the low rates of parasit-
to the nesting success of the host; these ism in many natural situations may be
parasites show both generalized and the result of natural selection favoring
very specialized host selection behaviors. behavior among the hosts to reduce
The cowbird Molothrus rufoaxillaris of parasitism because of its adverse effects.
tropical America parasitizes only the Many potential host species are known
cowbird Molothrus badius, while the to drive parasitic species away from
temperate Molothrus ater is known to their nests or nesting territories. Some
parasitize over 100 species. species can determine when a parasitic
Parasitism, particularly from cow- egg has been deposited in their nest and
birds and cuckoos, generally reduces the respond to it. Such species are called dis-
nest success of the hosts. In some cases, criminators, and they usually reject the
the existence of a single parasitic egg egg by throwing it from the nest, desert-
results in a total loss of the host’s young ing the nest, or building a new nest on
chapter 12

(see below), while in others it may cause top of the parasitized clutch. In contrast,
only partial loss. Because parasitism some species (acceptors) seem to be
is usually infrequent in populations (a unable to identify the foreign egg. The
sweeping survey found that about 3% selective action of discriminators against

384

1stPages_B.indd 384 7/22/20 11:55 AM

 alien eggs within their clutch results in
selection for egg mimicry; a discrimi-
nator cannot reject a parasite’s egg if it
cannot tell which egg is the intruder (fig.
12.12). Of course, a generalized parasite
like the Brown-headed Cowbird cannot
mimic the eggs of all 100 of its potential
hosts; it must succeed by having a high
survival rate with the few species for
which its egg is a mimic and by utiliz-
ing acceptor species. The specialized
parasitism of some species may reflect
their concentration on only host species
that their eggs mimic. An interesting,
though poorly understood, mechanism
to get around the problem of laying
mimetic eggs without being limited to a
single host occurs in some of the cuck-
oos. In these species, individual females
lay eggs that mimic the eggs of a partic-
ular species and selectively put them in
the appropriate host nests. Yet within a
parasitic species several races (termed
gentes, singular gens) may occur that
parasitize different hosts with different
egg types. The genetics involved in this
unusual pattern are not yet understood.
Another line of possible defense
might be for the host to peck the egg of
the parasite and remove it. Of course, if
Adaptive Variation in Avian Reproduction
the egg of the parasite mimics that of the
host, this is a problem. In addition, many
parasitic eggs have much harder shells
than the host eggs, such that a parent
attempting to peck a hole in the intrud-
ing egg may have its blow deflected by
the parasitic egg so that it bounces over
and punctures the host egg.
A final line of parental defense
against parasitism could occur after
Fig. 12.12. Examples of mimetic eggs laid by
hatching, if the young do not provide
cuckoos to match their hosts.
the proper stimuli for feeding or other
parental behavior. Because most pas-
serines have solid-colored mouthparts

385

1stPages_B.indd 385 7/22/20 11:55 AM

 when young, a good parasite should also Some recent work on cowbirds suggests
have such coloring. This is found in the that they also show this behavior in
parasitic cuckoos, even though non- some situations.
parasitic species have different-looking Most parasites lay eggs that develop
offspring. The viduine finches that para- rapidly, which gives them an early hatch
sitize estrildids mimic the mouth colors and advantages over their nest mates.
and markings and begging behaviors of There is some evidence that cuckoos lay
their estrildid hosts. an egg with a partly developed embryo
Brood parasites have evolved a to further aid development. Although
variety of responses to the protective growth rates of the nestlings are similar
adaptations of their potential hosts, as to those of their nest mates, many of
well as other adaptations to ensure their the parasites, particularly the cuckoos,
success. Parasitic cuckoos are large birds fledge at smaller sizes than their nest
(fig. 12.13) that apparently mimic hawks, mates. Cuckoos fledge at 50%–60%
a possible way for them to avoid being of adult body weight, while most pas-
chased away from potential nests. Cuck- serines fledge at near their parental
oos have been known to destroy a clutch
of eggs or kill a set of young, apparently
in order to get the parents to lay a new Fig. 12.13. A wagtail (Motacilla) feeding a
clutch that the cuckoo can parasitize. much larger young cuckoo (Cuculus).
chapter 12

386

1stPages_B.indd 386 7/22/20 11:55 AM

 weight. This gives the parasite further preadaptations in the evolution of brood
advantages in monopolizing parental parasitism. Because females will some-
care. Finally, some young parasites will times “dump” an egg in a nearby nest
kill nest mates. Young cuckoos push of a conspecific, that behavior has been
nest mates out using their back, while suggested as a pathway, but the shift
honeyguide young have a special point from facultative parasitism to obligate
on their bill that enables them to kill parasitism is difficult to understand. In
their nest mates. Parasitic species with some duck species in which individuals
such aggressive young usually lay just regularly lay eggs in the nests of other
one egg per nest, for obvious reasons. species, large “dump” nests sometimes
With the reduced costs of parental occur and are subsequently deserted by
care, many parasitic species have the the original nester.
potential for higher reproductive success Parasite-host interactions are often
than species that provide care. Estimates intricate, usually because of the potential
for total eggs laid in a season range up costs to the host. Among the viduine
to 25 for both cuckoos and cowbirds. finches, parasitic specialization on a par-
These may be laid in “clutches” of 2 to 5, ticular host species may involve not only
perhaps because their evolutionary pre- morphological adaptations such as the
decessors laid clutches of this size when appropriate markings on the nestlings,
nesting for themselves. Given that no but also some behavioral flexibility in
parental care is provided by either sex, such characteristics as learning of song.
it is not surprising that parasitic species In some viduines, males learn the song
are usually polygynous. of their host, which apparently serves
Some may show territorial behavior, as an attractant to females also reared
although others show primitive forms by that host. There is some evidence
of lekking. Some rather extreme forms that this vocal mimicry may be lead-
of sexual dimorphism occur among ing to speciation, perhaps without the
the parasitic viduine finches. Despite allopatric distributions usually required
all these adaptations that favor high for avian speciation (see chapter 4).
reproductive output in brood parasites, The viduine-estrildid interaction is also
Adaptive Variation in Avian Reproduction
they are generally no more successful unusual in that the parasitism is not
than nonparasitic forms. In general, the always detrimental to the host, an indi-
world is not overrun with brood para- vidual parasite might lay several eggs
sites, presumably because of the many in a single nest, and the young of both
defenses developed by host species. species are adapted to a diet of seeds.
Although many of the adaptations The recent expansion of the ranges
of parasite and host have been studied of several parasitic species has made
in detail, the steps in the evolution of studies on parasite-host interactions of
this strategy have not been uncovered. potential importance in avian manage-
Many species use previously used ment. We have already noted that popu-
nests, and some are known to take over lations already reduced in size by other
already constructed nests. This behavior, factors may be susceptible to increased
accompanied by the laying of an egg or nest parasitism. If long periods are
two, may have served as one of the first required for a species to adapt to parasit-

387

1stPages_B.indd 387 7/22/20 11:55 AM

 ism, such parasites may threaten their ground level. This is then covered with a
hosts with extinction. Understanding layer of soil. When the heat of decompo-
the variety of interactions and behavior sition approaches 29°C, females will lay
involved is therefore of both scientific their eggs in the vegetation. Although
and applied interest. the heat produced by decomposition
tends to remain around 33°C, climatic
Final Comments on conditions may alter the temperature,
Reproductive Behavior thereby affecting egg development. To
compensate for these changes, the male
The previous material has provided a regulates egg temperature by exposing
brief overview of the great variation in the eggs when cooling is needed or cov-
general reproductive behavior within ering them to protect them from colder
the world of birds. Given that there are conditions. He may also expose the eggs
only two sexes, an incredible number to direct sunlight when that is optimal.
of options seem to exist, particularly Experiments comparing male-manipu-
when we consider how strategies may lated nests with untended vegetation or
vary with the age of a bird, with its sand showed how well the male main-
population level, or with time during the tained nearly constant conditions. When
breeding season. the eggs hatch, the young dig their way
Despite the variations already out of the vegetation, dry off, and then
discussed, a few unusual reproductive go raise themselves, with no parental
behaviors have been omitted. One of care. In this situation, males are polyg-
the most unusual incubation patterns is ynous, mating with and getting eggs
that of the brush-turkeys or megapodes from multiple females, and females
(Megapodiidae), a group of gallinaceous are polyandrous, laying in the nests of
birds from the Australia–New Guinea multiple males. The EPP for such a sys-
region. Many of these accomplish incu- tem is related to the extreme precocial
bation by using the heat of decomposi- behavior of the young.
tion in mounds of decaying vegetation Another unusual behavior that is
or the heat stored by intensely radiated worth noting occurs in some of the
beach sand. While in some species hornbills. These cavity-nesting species
the eggs are simply deposited and left are unusual because the egg-laying
alone, in others the mound of vegeta- female is sealed into the cavity early in
tion is tended throughout incubation to the breeding cycle. From this time until
control the conditions in which the egg she leaves, when the nestlings are fairly
­develops. well grown, she depends on the male to
The classic study of mound tending bring her food. This seal is made of mud
was done on the Mallee Fowl (Leipoa and presumably serves as a predator
ocellata) of Australia (fig. 12.14).40 In deterrent. Food for the female during
this species, the male tends the mound incubation and brooding, as well as
chapter 12

for up to 11 months of the year. He food for the young during early nestling
excavates a pit 1 m by 3 m and then fills development, is provided by the male.
it heaping full with vegetation, until When the young are partly grown, the
the mound often reaches 60 cm above seal is broken and the female leaves the

388

1stPages_B.indd 388 7/22/20 11:55 AM

 Fig. 12.14. Structure of a nest of a Mallee Fowl that monogamy is anything but the
(Leipoa ocellata) (top), composed of both conservative, perhaps monotonous and
rotting vegetation and sandy soil. Temperature mundane system that it appears to be
Adaptive Variation in Avian Reproduction
control within the nest is shown as “natural” on the surface. Rather, subtle variations
and compared to an unregulated mound of occur among individuals with small
sand (control) and an unregulated mix of sand changes in age, population levels, envi-
and vegetation (artificial) (Frith 1956).
ronmental conditions, and experience.
With all the work in progress, continu-
nest; it is then resealed until time for the ing significant advances will be made in
young to fledge. our understanding of avian reproductive
Recent studies on reproductive strategies in the future.
behavior in birds have found that nearly
all species possess complex and inter-
esting behavior. Although the focus of
research has often been on nonmonoga-
mous systems because of their seeming
complexity, many authors have shown

389

1stPages_B.indd 389 7/22/20 11:56 AM

 C HA P T E R 13

Economic and Cultural

Values of Birds

B
irds play a valuable role in into dollar amounts. It is obvious that
nearly everyone’s life, but trying birds have an incredible value in our
to place some measure on this lives. Our goal in this chapter is to point
value is not always easy. While out some of the general ways that birds
it is possible to obtain data on how many affect our lives and provide us something
eggs are consumed in the United States of worth. Unfortunately, humans have
annually and to multiply that number by had many negative effects on birds, so
the average price to place a dollar value we end this chapter with a discussion of
on the input of eggs into our country’s these impacts and how we are trying to
economy, some equally real avian bene- reverse them in many cases.
fits are much more difficult to quantify.
How do we measure the value of each Domestication of Birds
grasshopper that a meadowlark eats in
a summer, or each weed seed eaten by a Many of the economic and cultural
goldfinch? Billions of birds eating insects values of birds are related to the ease
must have some economic impact, but with which birds can be domesticated.
how could that impact ever be fit into an Evidence suggests that domestication
economic analysis? goes back as far as 3000 BC.1 The Grey-
When we consider activities in which lag Goose (Anser anser) was most likely
people actively pursue birds in one form the first bird domesticated, followed
or another, similar problems result. We by the pigeon, Red Junglefowl (Gallus
can estimate the amount of money a gallus), and Mallard (Anas platyrhynchos)
hunter pays for gasoline, or a birder for in the Old World. New World civiliza-
birdseed and binoculars, but we cannot tions domesticated the Wild Turkey
translate into economic terms the emo- (Meleagris gallopavo) and Muscovy Duck
tional value of the time spent searching (Cairina moschata). Variations of these
for birds with either guns or binoculars. early forms continue to dominate our
Even more esthetic qualities, such as the bird production today, despite the devel-
birdsong that fills the woods on a spring opment and discovery of hundreds of
morning, the companionship of a pet forms of these domesticated species.
parakeet, or the beauty of a male cardinal Not just any bird is adaptable
on a snow-covered feeder, defy projection for domestication for food purposes.

390

1stPages_B.indd 390 7/22/20 11:56 AM

 Among the traits shared by most domes- Fig. 13.1. Some of the forms of chickens that
ticated species is the ability to be easily have been selected compared to the Red
fed, particularly when young. Thus, Junglefowl (Gallus gallus), the original
nearly all domesticated birds raised for chicken (Sossinka 1982).
food have precocial young, while those
with altricial young that are kept as that domestication does not remove
pets can often survive on a diet of seeds critical stimuli necessary for its suc-
when small. The breeding behavior of cessful completion. Species requiring
domesticated birds should be as flexible long aerial displays as part of pair-bond-
as possible. While this can sometimes ing would not be good candidates for
Economic and Cultural Values of Birds

be manipulated through artificial selec- domestication.

tion, it appears that the early adoption Among other behavioral attributes
of birds for domestication favored those valuable among birds selected for
species with flexible breeding seasons. domestication are imprinting and social-
In many cases, these were tropical or ity. Young that imprint on their captors
subtropical forms that were naturally and their environments are more easily
rather opportunistic breeders that controlled than young not showing
responded to rainfall or other short-term these traits. Species that live in groups
cues. Placed in captivity, these species or flocks make more successful domesti-
will breed over longer periods than most cated animals than those that are highly
temperate-breeding species, which have territorial.
limited breeding seasons. Reproduction Once a species has been domes-
should also be a simple enough process ticated, artificial selection for favored

391

1stPages_B.indd 391 7/22/20 11:56 AM

 traits can cause rather rapid change in achieve the most advantages of hyper-
the characteristics of the animal. For sexual birds, proper nutrition, disease
pet birds, selection may favor plumage control, and clean living conditions
or song traits that are deemed attrac- (including light regimes) to reach max-
tive. As we will see below, selection for imum growth must be provided. With
birds used for meat favors body size such conditions, farmers have been
and shape. Genetic changes require able to increase annual egg production
several generations to take effect. Over for laying hens and the size of chickens
the past few thousand years, the original and turkeys raised for meat (fig. 13.2).2
Red Junglefowl, which weighed about a In some cases, selection has resulted in
kilogram, has been selected into forms birds that become too large to walk at
that weigh well over 5 kg and include a relatively early stage, which requires
nearly all possible combinations of color, harvest earlier in life.
shape, and ornamentation (fig. 13.1).
Attempts at physiological change Birds and bird products
have generally focused on increasing
rates of productivity in domesticated There are a lot of chickens in the world.
birds, leading to a condition known as Estimates vary from 12 billion to 20 bil-
hypersexuality in many birds. Hyper-
sexual birds are distinctive for early
maturation and intense breeding. This Fig. 13.2. The effects of genetic selection and
is usually beneficial, as it leads to the improved care have increased the number of
acquisition of full size early in life, eggs produced by a hen each year (left) and
allowing farmers to obtain larger birds the weight of male turkeys at 26 weeks of age
for meat or more eggs from layers. To (right) (Phillips, Butler, and Sharp 1985).
Chapter 13

392

1stPages_B.indd 392 7/22/20 11:56 AM

 lion chickens worldwide.3 This is more required. The most successful caged
than the combined total of cats, dogs, birds, however, have been those that
pigs, cows, and rats. There are three readily adapt to breeding within cages.
chickens for every person on the planet. Among those are the Canary (Serinus
Perhaps the best available data canaria) and Budgerigar (Melopsittacus
regarding the value of birds in our lives undulatus, called parakeets in the United
are those associated with the economic States), which are able to feed seeds to
value of birds as food. The most recent their offspring.6 Raising insectivorous
data provided by the US Department of birds is more difficult; since most pet
Agriculture (USDA) for 2015 suggest owners want their bird to be an easy
that our economy spent $48 billion source of enjoyment, few insectivores or
on meat and eggs from poultry. This other predators serve as pets.
included $13.5 billion on eggs, $5.7 The popularity of caged birds in the
billion on turkey, and $28.7 billion on modern world has caused some prob-
chicken meat of various forms. Ameri- lems. The movement of many thousands
cans now consume four times as much of birds has served to transfer diseases
chicken as they did 60 years ago.4 that affect commercial birds. Among
The feather industry is much harder these, Newcastle disease is most famous.
to track in today’s world. Many feath- Because of this problem, the US gov-
ers are sold as decorations and as part ernment has strict laws about importing
of art projects, but tracing amounts is birds into this country. In some cases,
difficult. Feather pillows were once the escaped caged birds have established
rage, but currently many pillows use themselves in nonnative areas. While
artificial fillers. We know that as late as some of these use habitats that are not
1977, goose feathers worth $400 million acceptable to native birds, in some cases
were imported to the United States, but these exotics have the potential to cause
current figures are hard to find. real problems. The Monk Parakeet
(Myiopsitta monachus), which is a serious
Birds as pets agricultural pest in its native Argentina,
has fairly recently established itself in the
Domestication of birds for uses other United States. So far, it does not appear
Economic and Cultural Values of Birds

than food probably goes back as far as to have expanded its population or range
the domestication of the goose. Artificial as much as people originally thought it
selection has been practiced on such might. Tropical locations such as Puerto
species as the pigeon and canary for Rico often have large populations of
centuries, resulting in an enormous array introduced parrot species. While most
of varieties.5 With the development of air of these seem harmless and they often
travel in the past century, the variety of reside in highly disturbed urban areas
species available as pets has increased where native parrots no longer exist,
enormously. there is concern that these introduced
Domestication of birds for pets is a species might eventually expand their
somewhat easier process than domes- range and interact with the native Puerto
tication for food, particularly if only Rican Parrot (Amazona vittata), an
adult birds are kept and breeding is not extremely threatened species. Finally, in

393

1stPages_B.indd 393 7/22/20 11:56 AM

 some places, the pressure of the pet trade they will simply survive within the exotic
has resulted in collectors removing birds habitats that human disturbance has
from their native habitats faster than the caused. For example, around 30 spe-
birds can reproduce. This has been par- cies of African finches have established
ticularly true for some of the rare parrot populations on Puerto Rico, but most of
species found on tropical islands. Their them live in highly disturbed habitats
rarity makes them valuable to collectors, that are populated with plant species
but it also makes them susceptible to too that themselves come from Africa.
much collecting. The pet trade accen-
tuates this problem by often cutting Ecosystem Roles of Birds
down trees to get to the cavities where
the parrots nest, which may result in too Ecosystem characteristics involve energy
few nest sites for the parrots to be able to flow, trophic levels, and nutrient cycling.
maintain populations. Several parrots of Despite their large numbers and high
the Lesser Antilles are suffering because metabolic rates, birds apparently have
of the pet trade, although recent efforts rather small energetic roles in the tro-
to stop this have had some success, phic levels they occupy. Studies in forest
along with increased protection and the bird communities in both Illinois and
addition of artificial cavities for breeding Panama found that less than 1% of the
birds to use. total annual productivity went through
It is difficult to get accurate esti- the avian portion of the food chain.8
mates of how much money is involved Despite this low energetic role in the
in purchasing and supporting pets in the typical ecosystem, birds have important
world. The number of imported birds is effects on ecosystem function.
impressive. The port of Miami, Florida, The Millennium Ecosystem Assess-
handled over a half-million caged birds ment Group provided a four-category
in 1971. New York and Los Angeles may framework for assessing ecosystem
handle similar numbers. Even if only a roles of animals and their effects on
small percentage of these birds escape human well-being (2005). Provisioning
or are released by their owners, sizable services refer to natural products that
populations may result. Such releases are directly used by humans for food,
coupled with extensive habitat modifi- clothing, medicines, tools, or other uses.
cation may result in complex faunas of Cultural services provide recreation
introduced species. Although it is not opportunities, inspiration for art and
surprising that the tropical climates music, and spiritual values. Regulating
of Florida and California now support services include pest control and carcass
several dozen established populations removal. Supporting services, such as
of such introduced exotics as parrots, pollination, seed dispersal, water puri-
doves, and tropical finches, even New fication, and nutrient cycling, provide
York supports a dozen introduced parrot processes essential for ecological com-
species.7 It remains to be seen whether munities and agricultural ecosystems.
Chapter 13

these exotics will cause serious environ- Obviously, there is a great deal of varia-
mental problems through their interac- tion regarding the importance of birds
tions with the native fauna, or whether in filling these categories.

394

1stPages_B.indd 394 7/22/20 11:56 AM

 Those seed- or fruit-eating birds that Insectivorous birds are considered
serve as seed dispersers for plants play a the next-highest trophic level, as they
very important role in the ecosystem; the feed on insects that feed on plants. It is
effect of this dispersal may determine the exceedingly difficult to measure the value
structure of plant communities, particu- of birds as insect control agents, but one
larly in early-successional forests follow- estimate suggested that birds eat $1,500
ing some kind of disturbance. Among the worth of insects per hectare per year. A
trees that are most successful in coloniz- study in a coffee plantation estimated
ing an open field are those with bird-dis- that avian insectivory increased the farm-
persed fruits and seeds. Such fruits may er’s profit by $310 per hectare.12 The fact
vary from a tiny berry to an acorn or that insects have evolved so many ways
Brazil nut, but if birds eat them and pass to avoid bird predation certainly suggests
the seeds or deposit extra seeds in good that the effect of birds is pronounced. It
locations for germination, the plant will appears that some insects of the temper-
be favored by the interaction and forest ate zone have been able to avoid much of
community composition may be affected. this predation by periodic irruptions that
Because fruits are available all year in the swamp their avian predators. Since such
tropics, such fruit-bird interactions are irruptions are rare in the tropics, it is
much more common there than in the believed that avian insectivory there is an
temperate zone. They seem to reach their extremely potent force.
zenith with those species showing rather Predatory birds occupy the top tro-
tight mutualisms, such as the manakins phic level in the bird world. While they
discussed in chapter 12. Under certain may be thought of as having negative
circumstances, such mutualisms may value on those occasions when they prey
be important to the survival of one of the on other birds or beneficial animals, the
species. It has been suggested that birds dominant prey among most predatory
disperse the seeds of 92% of all tree and birds is rats and mice, which are nearly
woody species, plus those of thousands of always considered pests by humans.
other herbaceous plants.9 It has been estimated that a Barn Owl
Birds also interact with flowers in (Tyto alba) might eat 11,000 mice in its
valuable ways. The flowers of a great lifetime, which has a strong impact on
Economic and Cultural Values of Birds

many plants of the world have evolved mouse populations.13 It is difficult to

a shape to facilitate pollination by birds. prove that raptors can control prey num-
In the Old World, it has been suggested bers. In the case of rodents with cycling
that 3% to 5% of all plant species are abundance, it appears that raptors take
pollinated by birds.10 Even in the tem- advantage of these cycles but do not
perate zone of North America, it appears control them.
that there are at least 150 species of Scavenging birds such as condors
ornithophilous (bird-pollinated) plants and vultures provide important ecosys-
(fig. 13.3).11 Many species have come up tem services by removing the carcasses
with ways to cheat in these bird-flower of dead animals. While this is hard to
interactions, which has led to the many track quantitatively, it has been sug-
variations in flower shape, length, gested that these effects are massive.14
corolla strength, and other factors.

395

1stPages_B.indd 395 7/22/20 11:56 AM

 Fig. 13.3. Hummingbirds have different bill ment, according to those surveys. Many
sizes and shapes to match the flowers they use, outdoor enthusiasts combine hunting
which limits the mixing of nectar as a species for a variety of animals with fishing
goes from one flower to another. and other types of outdoor recreation. A
2016 survey suggested that as much as
Hunting for Game Birds $325 billion is spent overall on all these
types of hunting-related recreation.
A variety of different birds are hunted. As our society has advanced, hunt-
Many hunters focus on waterfowl (ducks ing for birds has become something
and geese), while others hunt upland done primarily for sport, rather than to
game birds such as doves, pheasant, and meet an actual need for food, as was the
quail. Surveys in 2011 suggested that case with earlier cultures. Most modern
about 16.5 million individuals over 16 hunters could buy their meat much more
years of age hunted for game birds and cheaply than hunt for it. With this shift
Chapter 13

spent around $25.6 billion doing so.15 in the motivation for hunting has come
Waterfowl hunters spent $663 million a strong antihunting sentiment among
on travel and $699 million on equip- people who feel that the killing for sport

396

1stPages_B.indd 396 7/22/20 11:57 AM

 of millions of birds annually is barbaric. highly dominant flock leaders, etc.) and
The morality of hunting in our modern the likelihood that these individuals
society is too complex an issue for us would have continued to live if not killed
to discuss in detail here. On behalf of by the hunter. These individual traits
hunting, it should be noted that nearly all contrast sharply with the general idea of
game species have been selected because a “harvestable surplus” that is often used
of their ability to maintain high popu- to justify hunting. Much support for
lations and thus provide annual sport an antihunting stance has come from
for the hunter. These species generally instances of abuse by hunters, as when
produce more young than can survive the individuals grossly exceed harvest limits,
winter, so hunting eliminates a portion make no attempt to locate wounded
of the population that would probably not game animals, or degrade their sur-
survive anyway. Through licenses and roundings in other ways. People holding
taxes, hunters support agencies that keep an antihunting philosophy generally feel
a close watch on these species so that that hunting is simply a primitive activ-
seasons can be regulated in a way that ity from our past that should be stopped.
protects these populations for future gen- There is obviously a middle ground
erations. In this way, hunters were really in this argument, which satisfies most
among the first conservationists, for reasonable people. Slob hunters that
they were among the first of the general abuse the privilege of hunting by
public to see that effort was necessary to exceeding limits, ignoring other people’s
protect our natural resources for future rights, and injuring animals with little
use. The many wildlife refuges that were regard for common decency should be
established using money gathered from stopped. But most hunters are not like
hunting fees have also been invaluable this. Rather, most are decent people
in protecting other, nongame species. who get tremendous pleasure from the
Only in recent years has the nonhunting whole process of hunting. To them, the
public been in a position to pay its share pursuit is as important as the actual kill,
of support for conservation. It is fright- if not more so. The time spent outdoors
ening to think how different the world searching for game is very special to
might be without the many areas pro- them, and the awareness of the natural
Economic and Cultural Values of Birds

tected by hunters before the development environment that they have developed
of an environmental ethic in the general has led to significant support for con-
public. servation. In some situations hunting
Antihunting arguments tend to is a necessary management tool to keep
focus on moral issues related to the populations from damaging the environ-
killing of animals for sport. They sug- ment. It is hard to envision an America
gest that it is incredibly chauvinistic to without hunting, for it is an important
justify taking an animal’s life for the few part of our culture. As long as hunters
minutes or hours of pleasure obtained maintain their generally high level of
by the hunting. Such arguments also appreciation and support for the envi-
focus on characteristics of the individ- ronments they use, this activity should
ual animals harvested (i.e., they may remain a part of our lives in the appro-
be members of lifelong breeding pairs, priate circumstances.

397

1stPages_B.indd 397 7/22/20 11:57 AM

 Bird-Watching and Feeding traits of distribution. The lab also runs
Project FeederWatch, in which amateur
Surveys suggest that as many as 45 birders send observations of birds at
million Americans watch birds in some their feeders to the lab for compilation
fashion, contributing $80 billion annu- and analysis, with results showing how
ally to the economy. Around $41 billion wintering birds vary from year to year
of this is spent on travel and equipment.16 and place to place.
An older survey suggests that as many as Many birders focus their activities
26 million people feed birds at home.17 on compiling giant lists of birds from
These enthusiasts spend over $500 all over the world. A variety of goals are
million on birdseed, $100 million on bird involved here, with “600 clubs” or “700
feeders, boxes, and baths, $18 million clubs” available for people who want to
on field guides or other books, and the see that many species north of Mexico,
majority of the $133 million that is spent or big years that involve the accumula-
each year on binoculars. Birds are an tion of a list of many thousands of spe-
important part of our lives and economy. cies across the world. Most regions have
a birding society that helps coordinate
Ornithological Societies and promote such lists and keeps them
consistent. In North America, the Amer-
Bird-watchers run the gamut from indi- ican Birding Association serves this
viduals who delight in putting scraps purpose, plus it develops its own official
on the porch for the local sparrows to list of species available for a regional list
hard-core field enthusiasts who revel or a big day/​month/​year list.
in their ability to instantly recognize as Many ornithological societies exist
many species as possible. The former across the world at a variety of levels.
may spend only a few dollars a year Most towns of any size have a local
on their activities, while the latter may bird club, usually one associated with
spend a small fortune. Many of the more the National Audubon Society. Such
dedicated bird-watchers become ama- local societies are often noteworthy for
teur scientists when they participate in running annual Christmas counts and
such efforts as Christmas Bird Counts attempting to bring knowledge of and
(run by the National Audubon Society), interest in birds to local schools.
regional distributional atlases (usually Most states have a state ornitholog-
coordinated by state agencies), or bird ical society or bird club. These often
censusing activities (coordinated by the meet only a few times a year but focus
US Geological Survey). In recent years, their annual activities on keeping track
the Cornell Lab of Ornithology has of the state’s birds. Most of these have
developed an incredible system of bird a checklist committee that keeps the
monitoring in a couple of ways. Its eBird official list for the state; most also have
system uses the records of up to 40,000 a journal that publishes information on
birders who send all their observations the state’s birds.
Chapter 13

to the lab, where they are compiled into A number of ornithological societies
impressive patterns of the timing and serve the goals and purposes of profes-
characteristics of migration and other sional ornithologists. Some of these are

398

1stPages_B.indd 398 7/22/20 11:57 AM

 regional and some international. The now. Normally, these changes in popu-
largest professional society is the Ameri- lations and extinctions are the result of
can Ornithological Society (AOS), which slow-moving, often widespread natu-
was formed when the former Ameri- ral processes such as natural climate
can Ornithologists’ Union and Cooper change, glacial movement, continental
Ornithological Society merged. Among drift, and so forth. Because these same
its duties, the AOS keeps the official processes often give rise to new species
list of species for both North and South (see chapter 4), an equilibrium between
America. It holds an annual meeting the loss of species and the evolution of
where scientists exchange ideas through new ones has often occurred.
plenary speeches, short talks, and infor- The last few centuries have seen a
mal interaction, often over a beverage. rapid expansion of the human popula-
The AOS currently publishes two jour- tion, both in total numbers and in the
nals (The Auk: Ornithological Advances area occupied. To support these rapidly
and The Condor: Ornithological Applica- increasing numbers, severe modifica-
tions) and a book series (Studies in Avian tion of most natural vegetation types has
Biology), but this may soon change. The occurred, generally with the replacement
Wilson Ornithological Society is smaller of native plant species and communities
in membership than the AOS and has with agricultural systems. Those bird spe-
a recent history of focusing its activities cies that could not adapt to these modi-
on ornithologists from smaller colleges. fied systems have often undergone severe
The Wilson Society publishes the Wilson population declines, with many going
Journal of Ornithology, which prints the extinct (see below). Conversely, species
most papers of any society and includes with adaptations that permitted them to
many short papers, which most journals use human-modified habitats have often
no longer do. The Association of Field shown great increases in numbers over
Ornithologists publishes the Journal time. In addition, increasing human pop-
of Field Ornithology, which may reflect ulations have caused reductions in many
its beginnings as a banding journal by bird populations through direct harvest-
focusing on field studies, although it ing of birds for food or other materials
publishes many good ornithological (such as feathers).
Economic and Cultural Values of Birds

papers. A variety of other societies exist, Whatever their causes, these popu-
most of which publish journals, with lation changes have been countered in
special focus on raptors, waterbirds, or some cases by human activities that can
regional patterns of distribution. generally be described as management.
Management refers to the manipulation
Bird Conservation and Management of habitat or other natural factors and
the control of human disturbance to
Changes in the populations of bird affect the populations of the managed
species over time are a natural part of species. While management can refer to
our world. Even the process of extinc- efforts to reduce the numbers of spe-
tion is natural; we discussed earlier cies that have become so numerous as
that there were more species of birds at to be pests, most management activ-
certain times in the past than there are ities are attempts to either maximize

399

1stPages_B.indd 399 7/22/20 11:57 AM

 the number of harvestable species or species can occur in all habitats. Some
protect the populations of threatened species seem to have evolved very
or endangered species. In other words, specialized habitat requirements. For
the term “management” most often example, the Kirtland’s Warbler (Seto-
implies some attempt at maximizing phaga kirtlandii) nests only in stands of
the populations or population growth Jack Pine (Pinus banksiana) of around
of a limited subset of species; most bird eight years of age.
species do not receive much in the way Presumably, birds have evolved a set
of management. of visual cues that tell them whether a
particular habitat is acceptable. Humans
Local Habitat Requirements can get some idea of what these cues
must be; good quail hunters can tell
For most bird species, population man- when they are in good quail habitat, just
agement is habitat management, where as experienced birders can often recog-
providing the proper vegetation condi- nize the sort of forest that would support
tions serves to increase the numbers of certain species of warblers. These impres-
the target bird species. Until recently, sions based on experience are of little
the focus of much research was on help, however, in designing management
determining the habitat requirements of practices, because they do not tell us what
managed species, such as habitat with the critical factors are that make a habitat
the proper qualities that could be pro- suitable for a particular species.
vided through management practices. A great deal of effort has been
Given that no bird species can live and invested in studies on how species select
breed in all habitat types, the provision habitats, because understanding this
of habitat of a quality that meets a bird’s is so critical to providing the proper
requirements is a minimum manage- habitats for managed species. Some of
ment goal. For any species, though, the first work done on correlating bird
populations can survive only if certain habitat selection and habitat characteris-
minimum requirements for the amount tics was done by Frances James in 1971
or location of this acceptable habitat are (fig. 13.4).18 She attempted to describe
met. Thus, habitat management for a the habitats selected by a variety of bird
species must include both local habitat species by using multivariate statistical
requirements and regional distributions analyses on a variety of measures of the
of these habitats, taking into account vegetation within each bird’s territory.
the movements of the species between Fifteen measures were taken within a
acceptable habitats. 0.1-acre circle within a bird’s territory
Most species of birds have a limited and usually centered on a male’s singing
set of habitats in which they can live. perch. Large samples of these vegetation
While some species with rather gener- measurements could then be analyzed in
alized requirements may occupy a wide a search for characteristics that defined
variety of a particular habitat type (for the preferred habitat of each species. In
Chapter 13

example, the Black-capped Chickadee particular, an effort was made to find

[Poecile atricapillus] is found in many those habitat attributes that were always
forest types throughout its range), no present in the habitats used by a species,

400

1stPages_B.indd 400 7/22/20 11:57 AM

 Fig. 13.4. Outline drawings of quantified
components of the habitats of six warbler
species in deciduous forest (James and
McCulloch 1985).

1stPages_B.indd 401 7/22/20 11:58 AM

 based on the supposition that those must without natural processes such as wind-
be critical requirements for the species. storms or fires. These clearings are often
Quantitative analyses of habitat not used by early-successional species for
selection by species have become more a year or two following the disturbance,
and more detailed since James’s pio- and such species may leave the area after
neering work. Virtually any modern 5 to 10 years as the forest regenerates.
research examining bird distribution or To manage for such early-successional
nesting success must include detailed species requires an active program that
habitat measures, although not all of creates early-successional forest, but
this research reaches the publication since such forest usually occurs at the
stage. Despite their apparent quantita- expense of cutting mature forest, forest
tive rigor, these descriptive techniques managers must engage in a balancing
are still difficult to convert into manage- act where management does not remove
ment applications for several reasons. mature forest at too rapid a rate relative
For example, even when we measure a to creating second-growth or edge forest.
variety of vegetative variables, we can-
not be sure that we have measured all Landscape Ecology: How Much
factors important to a target species. We Habitat Is Needed and Where
might discover that a species is always Does It Occur?
associated with mature forest canopy
but also requires small clearings where It is obvious that the first requirement
thick brush occurs. Focusing vegetation for managing a species is providing the
plots on the sites where males sing may proper habitat in which it can survive
be misleading. Studies have shown that and prosper. The next question is, how
singing males are often unpaired males, much of this habitat is required? We
so we may be measuring the habitat know that most species have territories
selection of unpaired males, while or home ranges, and it seems obvious
successfully nesting males are quiet and that a manager must provide enough of
not part of the vegetation study. Habitat the proper habitat to support at least one
selection may vary regionally, which territory or home range. But will an area
means a study in one area may not be that small always attract or maintain a
applicable to other sites. species, particularly if the acceptable hab-
Once some set of habitat conditions itat is a long distance from other accept-
is defined for a species, management able habitats? If an area large enough to
practices generally focus on providing support several pairs is provided, at what
this habitat in the managed area. For size do we know that we have enough
species adapted to mature vegetation habitat to support a local population, at
types such as climax forest or native least over some reasonable period?
grassland, management may focus just A variety of such questions can be
on the preservation of such habitats. asked about species that live only in spe-
Many species, though, require early-suc- cialized habitat types that are often found
Chapter 13

cessional habitats to nest; these habitats in small tracts widely separated from
often do not occur without active forest each other. Human land-use practices
management such as clear-cutting, or have tended to fragment such habitats as

402

1stPages_B.indd 402 7/22/20 11:58 AM

 forest and prairie, forcing many species land areas. In these cases, a species must
to exist in these patchy habitats. Under- be habitat specific to the extent that it
standing how to manage such species requires habitat types that are isolated
obviously requires some knowledge of by a “sea” of unsuitable habitats. Early
how long small populations can survive studies applied the equilibrium model
within a small isolated habitat type, and to either distinct habitat types (high-ele-
how members of small populations vation tundra on tropical mountains) or
disperse from one area to another. actual islands within large tropical lakes,
Surprisingly, studies of the bioge- but later studies showed that many spe-
ography of animals on tropical islands cies respond to the area of such habitats
have provided an approach that has as forests and prairies just as though they
greatly aided our understanding of were islands surrounded by water. These
the ecological factors at work in these studies were able to pinpoint species
isolated habitat types. As we mentioned whose behavioral and population charac-
in chapter 5, island biogeography has teristics resulted in their being sensitive
long looked at the factors that determine to area (termed area-sensitive species),
the number of species living together and in some cases the minimum areas
on islands. The discrete nature of island required to maintain viable populations
faunas, the differences in island size, the of these species could be estimated.
species-area relationship that is always Mainland island biogeographic studies
found in island systems, and the exis- differ from true island studies in that
tence of different archipelagoes make we must delineate those species whose
islands interesting natural experiments habitat requirements are fragmented or
in studies of factors shaping avian insular, and we must accept that there are
communities. The MacArthur-Wilson animals living in the habitats between the
equilibrium model provides a theoretical fragments (termed the matrix), and that
framework for understanding the factors these animals may interact with those
that form these communities. This in the fragments. Unlike on real islands,
model suggests that the number of spe- where the total number of land bird spe-
cies living on an island is the result of a cies decreases with island area, as habitat
balance between the rate at which new fragments get smaller, the number of
Economic and Cultural Values of Birds

species colonize the island and the rate species adapted to the specific habitat
at which established species go extinct. type may decline, but edge species may
Island size and isolation affect both increase in number, such that the total
rates, with big islands presumably able number of species is not affected in the
to both attract more species (because way it is on real islands. Because analyses
they are large targets) and maintain of these systems involve the distribution
populations of more species than small of habitats across larger areas (termed
islands (because big islands have more landscapes), approaches to such studies
space). Some of the evidence supporting have been defined as landscape ecology
this model was examined in chapter 5. rather than applied biogeography, even
A variety of studies have shown that though the basic principles of such stud-
the same dynamics apply to populations ies were originally derived from island
living in isolated habitat types in main- biogeography.

403

1stPages_B.indd 403 7/22/20 11:58 AM

 Dozens of studies of the effects of by an annual cycle that includes several
habitat fragmentation on bird distribu- months on the breeding grounds, which
tions have been done. Virtually all spe- is when the above patterns of manage-
cies that are habitat-interior specialists ment are critical. But we also noted that
show species-area curves, often requir- many migrants spend up to eight months
ing 100 or more hectares of habitat on a wintering ground where they are as
before they even occur within a habitat site faithful as they are during the breed-
fragment. In many cases, populations ing season. In addition, ­individual birds
in the smallest fragments have low must travel from breeding to wintering
rates of pairing success and little or no grounds and back, often using the same
reproductive success. Some of this nest sites from one year to the next.
failure is related to high rates of cow- Recognizing that management
bird parasitism in the habitat fragments might be needed to preserve distinctive
because of landscape-level cowbird pop- breeding habitat, winter habitat, and
ulation levels, but small fragments also stopover habitat through migration is
have high nest predation rates from one of the significant discoveries of the
snakes and other predators. These edge past 25 years. Managers must evaluate
effects are an important cause of the all the possible locations where popula-
area sensitivity seen in fragments; only tions might be limited and respond with
in fragments 300 ha or more in size do the appropriate management recom-
the habitat-­interior species have high mendations. For most long-distance
enough nest success rates to maintain migrants, such management involves
local populations. actions in at least two and often more
We are still trying to figure out the countries. In many cases, we do not
management implications of such bio- know the details of important aspects
geographic patterns. It is clear that hab- of the annual cycle. For example, the
itat fragments must be of sufficient size Kirtland’s Warbler we mentioned earlier
to negate the edge effects that dominate was known to winter in the Bahamas,
small fragments. Alternatively, if land- but only recently did we discover a
scapes support sufficient amounts of location where the birds can be found
nesting habitat, the birds using this hab- from one year to the next such that we
itat will be able to deal with the reduced can determine the important character-
rates of predation or parasitism that are istics needed for management, such as
the result of a landscape with mostly survival rate and site faithfulness. Since
nesting habitat. It is clear, though, that many long-distance migrants have been
modern land managers must be con- declining for the past 50 years, manag-
cerned with the regional arrangement of ing these migrants is a large challenge
both habitat type and habitat amount. for the future.

Migratory Birds and Full- Selected tools from the

Annual-­Cycle Management manager’s toolbox
Chapter 13

When we discussed migration, we noted To manage any bird population, we need

that many migrants are characterized detailed information on the demography

404

1stPages_B.indd 404 7/22/20 11:58 AM

 of that population, including habitat provision of nest boxes, as do many par-
requirements, movements, and survival rots. In this case, the predatory Pearly-
rates. Once the details of current limit- eyed Thrasher (Margarops fuscatus),
ing factors for a species are understood, another cavity nester, often preyed on
we can respond appropriately and per- parrot nests, but managers put up boxes
haps reverse any declines in that species’ that the thrashers preferred and located
population. Here we discuss some of them in such a way that the thrashers
the special tools that help a researcher served as sentries, protecting parrot
determine when limitation might occur nests from other thrashers.
and how these have been successful as Captive breeding. In some situations, lit-
management remedies. tle or no natural breeding is possible for
Tracking mechanisms. In discussing a species. In these cases, conservation-
migrant birds we showed the impor- ists have resorted to capturing most or
tance of knowing where individuals all of the remaining natural population
spend the whole year so that conser- and breeding that population in captiv-
vation responses can be applied in ity, with the hope that a large population
the right locations. In chapter 9 we can be developed in captivity at the same
discussed some of these, ranging from time as the natural habitat is restored
simple banding studies (which are and made safe for future reintroduction.
limited mostly to showing patterns of Not all species adapt to this methodol-
site fidelity for site-faithful species) to ogy, and it is almost always expensive,
studies of stable isotopes (which link but there are some success stories with
wintering sites with breeding sites). species such as the California Condor
Radio transmitters can follow individual (Gymnogyps californianus), a case where
birds but are limited in how far signals all the wild birds were captured and
can be followed. Geolocators track a bird put in cages for breeding. After a larger
through its annual cycle but require that population was achieved, birds were
the bird be caught at least twice. Satellite released in the wild, where there has
receivers are ideal for larger birds, but been some success.
the technology for these is getting better Conspecific attraction. In some cases, a
all the time. A recent study was able to species has become locally extinct but
Economic and Cultural Values of Birds

count penguins on breeding sites in managers have been able to provide what
Antarctica.19 New technology appears appears to be the appropriate habitat for
regularly, and in the next few years we its restoration. It appears that a species
should understand the details of migra- sometimes does not know how to col-
tion much more clearly. onize a new site, as in the past it relied
Artificial nests. The populations of many on breeding birds in a habitat to attract
species are limited because they are cav- new breeders. In many cases, managers
ity nesters, but cavities in many habitats have been able to use artificial decoys or
are limited in number. Provision of nest tapes of songs to attract new birds to an
boxes can quickly increase populations empty habitat. Hearing songs or seeing
in many cases. The Puerto Rican Par- decoys suggests to the new colonist that
rot (Amazona vittata) is a cavity-limited this site is being used, implying that it
species that responded positively to the is an acceptable place for the new bird

405

1stPages_B.indd 405 7/22/20 11:58 AM

 to breed. The Atlantic Puffin (Fratercula birds on earth are facing some chance of
arctica) went extinct on several nesting extinction.
islands off New England and showed no Patterns within these categories
signs of recolonizing those sites. Man- of extinct and threatened birds shed
agers put decoys along the coast where light on factors that make species more
nesting sites used to be, played puffin vulnerable (fig. 13.5).21 Since 1600, 93%
calls, and eventually attracted breeding of all extinctions have been of birds
birds. Tape-recorded calls have worked living on islands, and between 50%
for several other species to trick a breed- and 60% of the presently endangered
ing bird into thinking that a site had species are insular forms. This is not
successful breeding birds. surprising, as many island species have
small, endemic populations adapted to
Extinct and Endangered Species a limited area of habitats. These habitats
can easily be altered simply because
The impact of human activities has led of their small size. Additionally, many
to the extinction of many bird species island forms lived on islands where pre-
and left many others in danger of this dation was insignificant or nonexistent;
fate. To preserve species in the future, nonflying island species can rapidly go
we must understand the status of a spe- extinct with the introduction of preda-
cies, its population trends, and its hab- tors (including humans) to an island.
itat needs. On a worldwide basis, this Nest predation from rats, cats, or dogs
is done by the International Union for can also be devastating. Exotic diseases
Conservation of Nature (IUCN) with its have been known to affect native species
Red Data Book.20 The compilers of this in some cases. Introduced species can
book examine information on all species sometimes outcompete native forms
from throughout the world and list those on islands, while the effects of such
they believe need special attention. introduced grazers as pigs and goats can
The Red Data Book works from a modify native habitats to the detriment
total list of 10,284 existing bird species. of residents.
Since 1600, over 140 species are known Another general attribute of extinct
to have gone extinct, 17 are possibly species is that they are forest birds.
extinct, and 5 are extinct in the wild but Nearly two-thirds of extinct and endan-
live in captivity. There are 218 species gered species resided or reside in native
that are considered critically endangered forests, while wetland birds are the
and 416 species considered endangered, next most sensitive, with 12% of the
which means that around 6% of existing extinct species. Many fewer species have
birds are considered endangered or crit- suffered in grasslands, xeric forests, or
ically endangered. Although extinction brushy habitats because these areas are
is a natural process, this rate is much either kept in some form of grassland
higher than normal. The categories of under human agricultural practices or
vulnerable (741 species) and near threat- are similar to early-successional forest
Chapter 13

ened (971 species) add another 17% of types, communities that result from the
species of at least some concern, which destruction of mature forests. Species
suggests that nearly one-fourth of the specialized for habitats that require hun-

406

1stPages_B.indd 406 7/22/20 11:58 AM

 Economic and Cultural Values of Birds

Fig. 13.5. Relative importance of various causes primitive ancestor. Human involvement
of avian extinction since 1600 (Jackson 1977). in this area began with the settlement
of Polynesians over 1,000 years ago.22
These colonists undoubtedly quickly
dreds of years to recover from human caused the demise of a variety of nonfly-
disturbance are obviously the most ing forms, as a flightless goose or ibis
vulnerable to extinction. would be too easy a meal to pass up.
Of course, multiple factors may act This culture also began the process of
over time. As we noted in chapter 4, the habitat modification and the introduc-
Hawaiian Islands were renowned for tion of exotic predators, competitors,
the great diversity of forms that evolved and diseases. A long decline in the num-
within that island system from some ber of Hawaiian species started at this

407

1stPages_B.indd 407 7/22/20 11:58 AM

 time, although things did stabilize for a is evidence that many species that are
while. In the late 1700s, European settle- widespread and relatively abundant
ment brought with it new predators and have been showing long-term declines.
competitors, including feral goats, cats, Understanding such declines is critical
avian pox, and introduced birds, which for the conservation of such species. For
caused a jump in extinction. Just over example, the Partners in Flight program
100 years ago avian malaria occurred on in North America, which focuses on
the islands, which caused a final wave migratory birds, has produced con-
of extinction, although the archipelago siderable conservation effort to “keep
still has a variety of species that are just common birds common,” but many of
holding on. these target bird species show long-term
Much focus has been on the sta- declines across their limited ranges.
tus of endangered species, but there
Chapter 13

408

1stPages_B.indd 408 7/22/20 11:58 AM

 NOTES

Chapter 1 16. Nakane, Shimmura, Abe, and

Yoshimura, 2014.
1. Regal, 1975. 17. Ibid.
2. Brodkorb, 1971. 18. Winklhofer, 2012.
3. Hecht, Ostrum, Viohl, and Wellnhofer, 19. Mihailova, Berg, Buchanan, and Ben-
1985. nett, 2014.
4. Brush, 1986. 20. Konishi, 1969.
5. Heilman, 1927. 21. Konishi, 1973.
6. American Museum of Natural History, 22. Konishi, 1969.
2007. 23. Winklhofer, 2012.
7. Zheng, Zhou, Wang, et al., 2013. 24. Stalmaster and Gessaman, 1984.
8. Ostrum, 1979. 25. Kendeigh, Dol’nik, and Gavrilkov, 1977.
9. University of Montana, 2009. 26. Mugaas and King, 1981.
10. Foth, Tischlinger, and Rauhut, 2014. 27. Kendeigh, Dol’nick, and Gavrilkov,
11. Chiappe, 2007. 1977.
12. Dyke and Kaiser, 2011. 28. Ksepka, 2014.
13. Honovich, 2014.
14. Smith, Chiappe, Clarke, et al., 2015; Xu, Chapter 3
Zhou, Dudley, et al., 2014.
15. Quick and Ruben, 2009. 1. Pennycuick, 1975.
16. Feduccia, 2014. 2. Ksepka, 2014.
17. Wang, Zheng, O’Connor, et al., 2015. 3. Huey and Deutsch, 2016; Weimerskirch,
18. Feduccia, 2014. Bishop, Jeanniard-du-Dot, et al., 2016.
4. Morell, 2015; Waldron, 2014.
Chapter 2 5. Hertel, 1995; Campbell and Tonni, 1983.
6. Millener, 1989.
1. Welty, 1955. 7. James and Olson, 2004.
2. Regal, 1975. 8. Worthy and Scofield, 2012.
3. Clark, Elias, and Prum, 2011. 9. Holden, 2008.
4. Silcock, 2006. 10. Mlikovsky, 2003.
5. Howell and Pyle, 2015. 11. Andors, 1992.
6. Doucet, McDonald, Foster, and Clay 12. Blanco and Jones, 2005; Perkins, 2015.
2007.
7. Bishop, Spivey, Hawkes, et al., 2015. Chapter 4
8. Tucker, 1968.
9. Olson and Wiley, 2016. 1. Hanson, 2006, 2007.
10. Emery, 2006. 2. Lack, 1971; Cody, 1974.
11. Marzluff, Walls, Cornell, et al., 2010. 3. Ibid.
12. Wantanabe, 2010. 4. Cody, 1968.
13. Logan, Jelbert, Breen, et al., 2014. 5. MacArthur, 1958.
14. Morell, 2011. 6. Hespenheide, 1971.
15. Morrell, 2013. 7. Hutchinson, 1959.

409

1stPages_B.indd 409 7/22/20 11:58 AM

 8. Cody, 1968. 3. Schnell, 1970.
9. Terborgh, 1971; Terborgh and Weske, 4. Raikow, 1985.
1975. 5. Orians and Christman, 1968.
10. Grant, 197511. . 6. Raikow, 1987.
11. Schoener, 1983. 7. Sibley, 1973; Marten and Johnson, 1986;
12. Zink, 2002. Corbin, 1983.
13. Robbins, Braun, and Tobey, 1986. 8. Britten, 1986.
14. Emlen, Rising, and Thompson, 1975; 9. Sibley and Ahlquist, 1983.
­Kroodsma, 1975. 10. Sibley and Monroe, 1990.
15. Steadman, 1982. 11. Barker, Vandergon, and Lanyon, 2008.
16. Fleischer, James, and Olson, 2008. 12. Klicka, Fry, Zink, and Thompson, 2001.
13. Hackett, Kimball, Reddy, et al., 2008.
Chapter 5 14. Lovette, Pérez-Emán, Sullivan, et al.,
2010.
1. See the work of John Wiens, 1986. 15. Pennisi, 2014; Jarvis, Mirarab, Aberer, et
2. Willis, 1980. al., 2014.
3. Diamond, 1969. 16. Zhang, Li, Li, et al., 2014.
4. Diamond, 1975. 17. Prum, Berv, Dornburg, et al., 2015;
5. Connor and Simberloff, 1983. Thomas, 2015.
6. Diamond, 1975. 18. Zink, 2002; Petren, Grant, and Grant,
7. Sanderson, Diamond, and Pimm, 2011; 1999.
Collins, Simberloff, and Connor, 2011. 19. McKitrick and Zink, 1988.
8. Faaborg, 1982.
9. Ibid. Chapter 7
10. Terborgh and Faaborg, 1980.
11. Faaborg, 1982. 1. Schoener, 1968.
12. Simberloff and Boecklen, 1981; Case, 2. Yeaton and Cody, 1974.
Faaborg, and Sidell, 1983. 3. Gill and Wolf, 1975.
13. Abbott, Abbott, and Grant, 1977. 4. Stenger, 1958.
14. Terborgh and Faaborg, 1973. 5. Ewald and Carpenter, 1978.
15. Diamond, 1975. 6. Woolfenden and Fitzpatrick, 1975.
16. Faaborg, 1979. 7. Holmes and Sturges, 1975.
17. Ibid. 8. Verner, 1977.
18. Lein, 1972. 9. Orians and Willson, 1964.
19. Ibid. 10. Rich, 1978; Rice, 1978a.
20. Terborgh, 1971, 1985; Terborgh and 11. Clarke, 1984.
Weske, 1975. 12. Pulliam, Anderson, Misztal, and Moore,
21. Ibid. 1974.
22. Holmes, 1975; Holmes, Bonney, and 13. Rohwer and Butcher, 1988.
Notes to Pages 99–214

Pacala, 1979. 14. Johnston and Fleischer, 1981.

23. Robinson and Holmes, 1982. 15. Hutto, 1994.
24. Holmes and Recher, 1986. 16. Munn, 1985.
17. Thiollay and Jullien, 1998.
Chapter 6 18. Tinbergen, 1981.
19. Krebs, Stephens, and Sutherland, 1977.
1. Feduccia, 1977. 20. Goss-Custard, 1977.
2. Ibid. 21. Davies, 1977.

410

1stPages_B.indd 410 7/22/20 11:58 AM

 22. Bryant and Turner, 1982. 9. Fitzpatrick, 1980.
23. Krebs and Avery, 1985. 10. Ketterson and Nolan, 1976.
24. Tinbergen, 1981. 11. Ibid.
25. Drent, 1978. 12. Ruppell, 1944.
13. DeLuca, Woodworth, Rimmer, et al.,
Chapter 8 2015.
14. Bishop, Spivey, Hawkes, et al., 2015.
1. Kirk and Mossman, 1998. 15. DeLuca, Woodworth, Rimmer, et al.,
2. James, 1970. 2015.
3. Aldrich, 1984. 16. Deppe, Ward, Bolus, et al., 2015; Bus-
4. Turcek, 1966. kirk, 1968, 1980.
5. Hamilton and Heppner, 1967. 17. Ibid.
6. Burtt, 1986. 18. Gauthreaux, Michi, and Belser, 2005.
7. Kendeigh, 1961. 19. Deppe, Ward, Bolus, et al., 2015; Bus-
8. White, Bartholomew, and Howell, 1975. kirk, 1968, 1980.
9. Chaplin, 1982. 20. Gauthreaux, Michi, and Belser, 2005.
10. Ohmart and Lasiewski, 1971. 21. Farner, 1955.
11. Dawson and Carey, 1976. 22. Alerstam, 1981.
12. Wolf and Hainsworth, 1972. 23. Perdeck, 1958.
13. Lasiewski, 1963. 24. Mazzeo, 1953.
14. Withers, 1977. 25. Keeton, 1969, 1974.
15. Johansen and Millard, 1973. 26. Emlen, 1967.
16. Whittow, 1986b. 27. Wiltschko, 1968, 1972.
17. Lustick, Adam, and Hinko, 1980. 28. Fretwell, 1980.
18. Bartholomew and Dawson, 1979. 29. Ibid.
19. Lasiewski, 1969. 30. Karr, 1976.
20. Phillips, Butler, and Sharp, 1985. 31. Cox, Thompson, Cox, and Faaborg,
21. Schmidt-Nielsen, 1959. 2014.
22. Skaudhage, 1981. 32. Keast and Morton, 1980; Hagan and
23. Thomas, 1982. Johnston, 1992; Greenberg and Marra,
24. Skaudhage, 1981. 2005.
25. Phillips, Butler, and Sharp, 1985. 33. Hobson, Van Wilgenburg, Faaborg, et
26. Johnson, van Riper, and Pearson, 2002. al., 2014.
27. Balda, 1980. 34. Cox, Thompson, Cox, and Faaborg,
28. Kamil and Balda, 1985. 2014.
35. Sherry and Holmes, 1992.
Chapter 9 36. McKinnon, Fraser, and Stutchbury,
2013.
1. Contina, Bridge, Seavy, et al., 2013.
Notes to Pages 217–295

2. Jahn, Cuerto, Fox, et al., 2013. Chapter 10

3. Rappole, Morton, Lovejoy, and Ruos,
1983. 1. Romanoff and Romanoff, 1949.
4. Gill, Tibbitts, Douglas, et al., 2009. 2. King, Buillard, Garrett, et al., 2002.
5. Myers, 1980. 3. Witschi, 1935.
6. MacArthur, 1959; Willson, 1976. 4. Schulze-Hagen, Leilser, Birkhead, and
7. Moreau, 1972. Dyrcz, 1995.
8. Keast, 1980. 5. Ekstrom, Burke, Randrianaina, and

411

1stPages_B.indd 411 7/22/20 11:58 AM

 ­ irkhead, 2007; Pitcher, Dunn, and
B 15. Weeks, 1978.
Whittingham, 2005. 16. Grasse, 1950.
6. McCracken, 2000. 17. Byrkjedal, 1987.
7. Drent, 1975. 18. Van Tyne and Berger, 1976.
8. O’Connor, 1984. 19. Kluijver, 1950.
9. Drent, 1975. 20. Tinbergen, 1951.
10. Russell, 1969. 21. von Haartman, 1949.
11. Drent, 1975. 22. Grundel, 1987.
12. Carey, 1980a.
13. Hauber, 2014. Chapter 12
14. Oniki, 1985.
15. Carey, 1980b. 1. Willis, 1980.
16. Drent, 1975. 2. Ricklefs, 1980.
17. Rahn and Ar, 1974. 3. Grant, 1985.
18. Bock and Hikida, 1968. 4. Perrins, 1965, 1980; Perrins and Moss,
19. Vince, 1969. 1975.
20. Sotherland and Rahn, 1987; Ricklefs, 5. Cody, 1966.
1983. 6. Howe, 1976.
21. O’Connor, 1984. 7. McGillivray, 1983.
22. Perrins, 1976. 8. Chapin and Wing, 1959.
23. Morton and Carey, 1971. 9. Parker and Burley, 1998.
24. Cox, Thompson, Cox, and Faaborg, 10. Conrad, Robertson, and Boag, 1998;
2014. Stutchbury and Morton, 2008.
25. Shefte, Bruggers, and Schafer, 1982. 11. Calhim and Birkhead, 2006.
26. Benoit and Ott, 1944. 12. Orians, 1969.
27. Bunning, 1963. 13. Verner and Willson, 1966.
28. Hamner, 1963. 14. von Haartman, 1969.
29. Meier and Ferrell, 1978. 15. Weller, 1980.
30. Murton and Westwood, 1977. 16. Wiley, 1973; Lill, 1974.
31. Farner and Gwinner, 1980. 17. Johnsgard, 1983.
18. Van Rhijn, Jukema, and Piersma, 2014.
Chapter 11 19. Blomqvist, Wallander, and Andersson,
2001.
1. Dhondt, Schillemans, and De Laft, 1982. 20. Oring, 1986.
2. Darling, 1938. 21. Jenni, 1974.
3. Krebs, 1977. 22. Hays, 1972.
4. Morton, 1970. 23. Pitelka, Holmes, and MacLean, 1964.
5. Falls, 1969. 24. Vehrencamp, 1977; Emlen and Vehren-
Notes to Pages 296–392

6. Kroodsma, 1982. camp, 1983.

7. Kroodsma, 1985. 25. Stacey and Koenig, 1984.
8. Nottebohm, 1975. 26. Ligon and Ligon, 1982.
9. Thorpe, 1961. 27. Woolfenden and Fitzpatrick, 1978,
10. Kroodsma, 1986. 1984.
11. Rice, 1978b. 28. Ligon and Ligon, 1978.
12. Stiles, 1982. 29. Gayou, 1986.
13. Wagner, 1954. 30. Vehrencamp, 1977; Emlen and Vehren-
14. Calder, 1973. camp, 1983.

412

1stPages_B.indd 412 7/22/20 11:58 AM

 31. Faaborg, de Vries, Patterson, and Grif- 5. Sossinka, 1982.
fin, 1980. 6. Ibid.
32. Ridpath, 1972. 7. USDA, 2016.
33. Elie, Mathevon, and Vignal, 2011; Con- 8. Millennium Ecosystem Assessment,
over and Hunt, 1984. 2005.
34. Dunn and Cockburn, 1997. 9. Johnson, Kellerman, and Stercho, 2010.
35. Houston and Davies, 1985. 10. Grant and Grant, 1968.
36. Weller, 1967. 11. Ibid.
37. Morel, 1973. 12. Johnson, Kellerman, and Stercho, 2010.
38. Lack, 1963; Payne, 1977. 13. Wood and Fee, 2003.
39. Ortega, Cruz, and Mermoz, 2005. 14. DeVault, Rhodes, and Shivik, 2003.
40. Frith, 1956. 15. US Fish and Wildlife Service, 2018a.
16. US Fish and Wildlife Service, 2018b.
Chapter 13 17. Kellert, 1980.
18. James and McCulloch, 1985.
1. Sossinka, 1982. 19. Ancel, Cristofari, Fretwell, et al., 2014.
2. Phillips, Butler, and Sharp, 1985. 20. Jackson, 1977.
3. Lawler, 2014; Cocker, 2013. 21. Ralph and van Riper, 1985.
4. Ibid. 22. Ibid.

Notes to Pages 393–407

413

1stPages_B.indd 413 7/22/20 11:58 AM

1stPages_B.indd 414 7/22/20 11:59 AM
 BIBLIOGRAPHY

Abbott, I., L. K. Abbott, and P. R. Grant. Bartholomew, G. A. 1977. Energy

1977. Comparative ecology of Galapa- ­metabolism. In Animal Physiology:
gos ground finches (Geospiza Gould): ­Principles and adaptations, ed. M.
Evaluation of the importance of floristic S. ­Gordon, pp. 57–100. New York:
diversity and interspecific competition. ­Macmillan.
Ecological Monographs 47:151–84. Bartholomew, G. A., and W. R. Dawson.
Aldrich, J. W. 1984. Ecogeographic vari- 1979. Thermoregulatory behavior
ation in size and proportions of during incubation in Heermann’s
Song Sparrows (Melospiza melodia). Gulls. ­Physiological Zoology 52:422–37.
­Ornithological Monographs 35:1–34. Benoit, J., and L. Ott. 1944. External and
Alerstam, T. 1981. The course and timing internal factors in sexual activity: Effect
of bird migration. In Animal Migration, of irradiation with different wave-
ed. J. Aidley, pp. 9–54. Cambridge: lengths on the mechanisms of photo­
­Cambridge University Press. stimulation of the hypophysis and
American Museum of Natural History. on testicular growth in the immature
2007. Velociraptor had feathers. Sci- duck. Yale ­Journal of Biological Medicine
enceDaily, September 20. 17:27–46.
Ancel, A., R. Cristofari, P. T. Fretwell, P. N. Bertram, B. C. R. 1980. Vigilance and
Trathan, B. Wienecke, M. Boureau, J. group size in ostriches. Animal
Morinay, S. Blanc, Y. Le Maho, and C. Behaviour 28:278–86.
Le Bohec. 2014. Emperors in hid- Binkley, S., E. Kluth, and M. Menaker. 1971.
ing: When ice-breakers and satellites Pineal function in sparrows: Circadian
complement each other in Antarctic rhythms and body temperature. Science
exploration. PloS ONE 9:e100404. 174:311–14.
Andors, V. A. 1992. Reappraisal of the Birkhead, T. 2012. Bird Sense. New York:
Eocene groundbird Diatryma (Aves: Walker.
Anserimorphae). Los Angeles County Bishop, C. M., R. J. Spivey, L. A. Hawkes,
Museum of Natural History, Science N. Batbayar, B. Chua, P. B. Frappell,
Series 36:109–26. W. K. Milsom, et al. 2015. The roller
Ar, A., B. Ariels, A. Belinsky, and Y. Yom coaster flight strategy of bar-headed
Tov. 1987. Energy in avian eggs and geese conserves energy during Hima-
hatchlings: Utilization and transfer. layan migrations. Science 347:250–54.
Journal of Experimental Zoology 1:154– Blanco, R. E., and W. W. Jones. 2005. Terror
64. birds on the run: A mechanical model
Balda, R. P. 1980. Are seed-caching to estimate its maximum running
­systems co-evolved? Acta Congressus speed. Proceedings of the Royal Society B
Internationalis Ornithologici 2:1185–91. 272:1769–73.
Barker, F. K., A. J. Vandergon, and S. M. Blomqvist, D., J. Wallander, and M. Anders-
Lanyon. 2008. Assessment of species son. 2001. Successive clutches and
limits among Yellow-breasted Mead- parental roles in waders: The impor-
owlarks (Sturnella spp.) using mito- tance of timing in multiple clutch sys-
chondrial and sex-linked markers. Auk tems. Biological Journal of the Linnean
125:869–79. Society 74:549–55.

415

1stPages_B.indd 415 7/22/20 11:59 AM

 Bock, W. J. 2015. Book Review: Riddle of the during nesting of hummingbirds in the
Feathered Dragons. Wilson Journal of Rocky Mountains. Ecology 54:127–34.
Ornithology 127:344–46. Calhim, S., and T. R. Birkhead. 2006.
Bock, W. J., and R. S. Hikida. 1968. An Testes size in birds: Quality versus
analysis of switch and tonus fibers in ­quantity—assumptions, errors, and
the hatching muscle. Condor 70:211–22. ­estimates. Behavioral Ecology 18:271–75.
Britten, R. J. 1986. Rates of DNA-sequence Campbell, K. E., and E. P. Tonni. 1983. Size
evolution differ between taxonomic and locomotion in the teratorns (Aves:
groups. Science 231:1393–98. Teratornithidae). Auk 100:390–403.
Brodkorb, P. 1971. Origin and evolution of Carey, C. 1980a. Adaptation of the avian
birds. In Avian Biology, vol. 1, ed. D. S. egg to high altitude. American Zoologist
Farner and J. R. King, pp. 19–55. New 20:449–59.
York: Academic Press. ———. 1980b. Ecology of avian
Brown, J. L. 1964. The evolution of diver- ­reproduction. BioScience 30:819–24.
sity in avian territorial systems. Wilson Case, T. J., J. Faaborg, and R. Sidell. 1983.
Bulletin 76:160–69. The role of body size in the assembly of
Brush, A. H. 1986. The beginnings of West Indian bird communities. Evolu-
birds. Auk 103:838–39. tion 37:1062–74.
Bryant, D. M., and A. K. Turner. 1982. Catchpole, C. K. 1982. The evolution of bird
Central place foraging by swallows song in relation to mating and spacing
(Hirundinidae): The question of load behavior. In Acoustic Communication
size. Animal Behaviour 30:845–56. in Birds, ed. D. E. Kroodsma and E. H.
Bunning, E. 1963. The Physiological Clock: Miller, pp. 297–319. New York: Aca-
Endogenous Diurnal Rhythms and demic Press.
Biological Chronometry. Berlin: Spring- Chapin, J. P., and L. W. Wing. 1959. The
er-Verlag. Wideawake Calendar, 1953 to 1958. Auk
Burtt, E. H., Jr. 1986. An analysis of phys- 76:153–58.
ical, physiological, and optical aspects Chaplin, S. B. 1982. The energetic signif-
of avian coloration with emphasis on icance of huddling behavior in Com-
wood warblers. Ornithological Mono- mon Bushtits (Psaltriparus minimus).
graphs 38:1–126. Auk 99:424–30.
Buskirk, W. H. 1968. The arrival of trans- Chiappe, L. M. 2007. Glorified Dinosaurs:
Gulf migrants on the northern coast of The Origin and Early Evolution of Birds.
Yucatan in fall. Master’s thesis, Louisi- New York: John Wiley and Sons.
ana State University, Baton Rouge. Clark, C. J., D. O. Elias, and R. O. Prum.
———. 1980. Influence of meteorological 2011. Aeroelastic flutter produces
patterns and trans-Gulf migration on hummingbird feather songs. Science
the calendars of latitudinal migrants. 333:1430–33.
In Migrant Birds in the Neotropics: Ecol- Clarke, M. F. 1984. Interspecific aggres-
ogy, Behavior, Distribution, and Conser- sion within the genus Manorina. Emu
vation, ed. A. Keast and E. S. Morton, 84:113–15.
pp. 485–91. Washington, DC: Smithso- Clements, J. F. 2007. The Clements Checklist
nian Institution Press. of Birds of the World. 6th ed. Ithaca, NY:
Bibliography

Byrkjedal, L. 1987. Antipredator behav- Cornell University Press.

ior and breeding success in Greater Cocker, Mark. 2013. Birds and People. Lon-
Golden-plover and Eurasian Dotterel. don: Jonathan Cape.
Condor 89:40–47. Cody, M. L. 1966. A general theory of
Calder, W. A. 1973. Microhabitat selection clutch size. Evolution 20:174–84.

416

1stPages_B.indd 416 7/22/20 11:59 AM

 ———. 1968. On the methods of resource Dawson, W. R., and C. Carey. 1976. Sea-
division in grassland bird communi- sonal acclimation to temperature in
ties. American Naturalist 102:107–47. cardueline finches: I. Insulative and
———. 1974. Competition and the Structure metabolic adjustments. Journal of Com-
of Bird Communities. Princeton, NJ: parative Physiology 12:317–90.
Princeton University Press. DeLuca, W. V., B. K. Woodworth, C. C.
Collins, M. D., D. Simberloff, and E. F. Rimmer, P. P. Marra, P. D. Taylor, K. P.
Connor. 2011. Binary matrices and McFarland, S. A. Mackenzie, and D. R.
checkerboard distributions of birds Norris. 2015. Transoceanic migration
of the Bismarck Archipelago. Journal by a 12 g songbird. Biology Letters 11.
of Biogeography 38. doi:10.1111/​j.1365– doi:10.1098/​rsbl.2014.1045.
2699.2011.02506.x. Deppe, J. L., M. P. Ward, R. T. Bolus, R. H.
Connor, E. F., and D. S. Simberloff. 1983. Diehl, A. Celis-Murillo, T. J. Zenzal Jr.,
Interspecific competition and species F. R. Moore, et al. 2015. Fat, weather,
co-occurrence patterns on islands: Null and date affect migratory songbirds’
models and the evaluation of evidence. departure decisions, routes, and
Oikos 41:455–65. crossing times in the Gulf of Mexico.
Conover, M. R., and G. L. Hunt. 1984. Proceedings of the National Academy of
Experimental evidence that female-fe- Sciences 112:E6331–E6338. doi:10.1073/​
male pairs in gulls result from a pnas.1503381112.
shortage of breeding males. Condor DeVault, T. L., O. E. Rhodes, and J. A. Shi-
86:472–76. vik. 2003. Scavenging by vertebrates:
Conrad, K. F., R. J. Robertson, and P. T. Behavioral, ecological, and evolutionary
Boag. 1998. Frequency of extrapair perspectives on an important energy
young increases in second broods of transfer pathway in terrestrial ecosys-
Eastern Phoebes. Auk 115:497–502. tems. Oikos 102:225–34.
Contina, A., E. S. Bridge, N. E. Seavy, J. M. Dhondt, A. A., J. Schillemans, and J. De
Duckles, and J. F. Kelly. 2013. Using Laft. 1982. Blue Tit territories: I. Popu-
geologgers to investigate bimodal lations at different density levels. Ardea
isotope patterns in Painted Buntings 70:185–88.
(Passerina ciris). Auk 130:265–72. Diamond, J. M. 1969. Avifaunal equilib-
Corbin, K. W. 1983. Genetic structure and ria and species turnover rates on the
avian systematics. In Current Orni- Channel Islands of California. Proceed-
thology, vol. 1, ed. R. F. Johnston, pp. ings of the National Academy of Sciences
211–44. New York: Plenum. 64:57–63.
Cox, W. A., F. R. Thompson III, A. Cox, and ———. 1975. Assembly of species com-
J. Faaborg. 2014. Post-fledging survival munities. In Ecology and Evolution of
in passerine birds and the value of post Communities, ed. M. L. Cody and J. M.
-fledging studies to conservation. Journal Diamond, pp. 342–444. Cambridge,
of Wildlife Management 78:183–93. MA: Harvard University Press.
Darling, F. F. 1938. Bird flocks and the ———. 1979. Niche shifts and the redis-
breeding cycle: A contribution to the covery of interspecific competition.
study of avian sociality. Cambridge: American Scientist 66:322–31.
Bibliography

Cambridge University Press. ———. 1982. Evolution of bowerbirds’

Davies, N. B. 1977. Prey selection and bowers: Animal origins of the aesthetic
social behavior in wagtails (Aves: sense. Nature 297:99–102.
Motacillidae). Journal of Animal Ecology Doucet, S. M., D. B. McDonald, M. S.
46:37–57. Foster, and R. P. Clay. 2007. Plumage

417

1stPages_B.indd 417 7/22/20 11:59 AM

 development and molt in Long-tailed of mating systems. Science 197:215–23.
Manakins (Chiroxiphia linearis): Vari- Emlen, S. T., J. D. Rising, and W. L.
ation according to sex and age. Auk Thompson. 1975. A behavioral and
124:29–43. morphological study of sympatry in
Drent, R. H. 1975. Incubation. In Avian the Indigo and Lazuli Buntings of the
Biology, vol. 5, ed. D. S. Farner, J. R. Great Plains. Wilson Bulletin 87:145–77.
King, and K. C. Parkes, pp. 333–420. Emlen, S. T., and S. L. Vehrencamp. 1983.
New York: Academic Press. Cooperative breeding strategies among
———. 1978. Investeren in nakomel- birds. In Perspectives in Ornithology, ed.
ingschap (Investment in offspring). A. H. Brush and G. A. Clark Jr., pp.
­Inaugural lecture, Groningen, Nether- 93–133. Cambridge: Cambridge Univer-
lands. sity Press.
Dugger, K. M., J. Faaborg, W. J. Arendt, and Ewald, P. W., and F. L. Carpenter. 1978.
K. A. Hobson. 2004. Understanding Territorial responses to energy manip-
survival and abundance of overwin- ulations in the Anna Hummingbird.
tering warblers: Does rainfall matter? Oecologia 31:277–92.
Condor 106:744–60. Faaborg, J. 1979. Qualitative patterns
Dunn, P. O., and A. Cockburn. 1997. Costs of avian extinction on Neotropical
and benefits of extra-group paternity land-bridge islands. Journal of Applied
in Superb Fairy-wrens. Ornithological Ecology 16:99–107.
Monographs 49:147–61. ———. 1982. Trophic and size structure
Dyke, G., and G. Kaiser. 2011. Living of West Indian bird communities.
Dinosaurs: The Evolutionary History of Proceedings of the National Academy of
Modern Birds. West Sussex, England: Sciences 79:1563–67.
John Wiley and Sons. Faaborg, J., T. de Vries, C. B. Patterson,
Ehrlich, P. R., D. S. Dobkin, and D. Wheye. and C. R. Griffin. 1980. Preliminary
1988. The Birder’s Handbook. New York: observations on the occurrence and
Simon and Schuster. evolution of polyandry in the Galapa-
Ekstrom, J. M. M., T. Burke, L. Randri- gos Hawk (Buteo galapagoensis). Auk
anaina, and T. R. Birkhead. 2007. 97:581–90.
Unusual sex roles in a highly promis- Falls, J. B. 1969. Function of territorial
cuous parrot: The Greater Vasa Parrot song in the White-throated Sparrow.
Caracopsis vasa. Ibis 149:313–20. In Bird Vocalizations, ed. R. A. Hinde,
Elie, J. E., N. Mathevon, and C. Vignal. 2011. pp. 207–32. Cambridge: Cambridge
Same-sex pair-bonds are equivalent to ­University Press.
male-female bonds in a life-long socially Farner, D. S. 1955. The annual stimulus for
monogamous songbird. Behavioral Ecol- migration: Experimental and physiolog-
ogy and Sociobiology 65:2197–2208. ical aspects. In Recent Studies in Avian
Emery, N. J. 2006. Cognitive ornithology: Biology, ed. A. Wolfson, pp. 198–237.
The evolution of avian intelligence. Urbana: University of Illinois Press.
Philosophical Transactions of the Royal Farner, D. S., and E. Gwinner. 1980. Photo-
Society B 361:23–43. periodicity, circannual, and reproduc-
Emlen, S. T. 1967. Migratory orientation of tive cycles. In Avian Endocrinology, ed.
Bibliography

the Indigo Bunting Passerina cyanea. I. A. Epple and M. H. Stetson, pp. 331–36.
Evidence for use of celestial cues. Auk New York: Academic Press.
84:309–42. Feduccia, A. 1977. A model for the
Emlen, S. T., and L. W. Oring. 1977. Ecol- ­evolution of perching birds. Systematic
ogy, sexual selection, and the evolution Zoology 26:19–31.

418

1stPages_B.indd 418 7/22/20 11:59 AM

 ———. 2002. Birds are dinosaurs: ­Simple numbers. In Migrant Birds in the Neo-
answer to a complex question. Auk tropics: Ecology, Behavior, Distribution,
119:1187–201. and Conservation, ed. A. Keast and E. S.
———. 2012. Riddle of the Feathered Morton, pp. 517–28. Washington, DC:
­Dragons: Hidden Birds of China. New Smithsonian Institution Press.
Haven, CT: Yale University Press. Frith, H. J. 1956. Temperature regulation
———. 2013. Bird origins anew. Auk in the nesting mounds of the Mal-
130:1–12. lee-Fowl, Leipoa ocellata Gould. CSIRO
———. 2014. Avian extinction at the end of Wildlife Research 1:79–95.
the Cretaceous: Assessing the magni- Gause, G. F. 1934. The Struggle for Existence.
tude and subsequent explosive radia- New York: Hafner.
tion. Cretaceous Research 50:1–15. Gauthreaux, S. A., Jr., J. E. Michi, and C.
Feduccia, A., and S. A. Czerkas. 2015. G. Belser. 2005. The temporal and
Testing the neoflightless hypothesis: spatial structure of the atmosphere
Propatagium reveals flying ancestry of and its influence on bird migration
oviraptorosaurs. Journal of Ornithology strategies. In Birds of Two Worlds, ed. R.
156. doi:10.1007/​s10336-015-1190-9. Greenberg and P. P. Marra, pp. 182–93.
Feduccia, A., L. D. Martin, and S. Tarsitano. Baltimore: Johns Hopkins University
2007. Archaeopteryx: Quo vadis? Auk Press.
124:373–80. Gayou, D. C. 1986. The social system of the
Fitzpatrick, J. W. 1980. Wintering of North Texas Green Jay. Auk 103:540–47.
American tyrant flycatchers in the Gill, F. B., and L. L. Wolf. 1975. Economics
Neotropics. In Migrant Birds in the Neo- of feeding territoriality in the Gold-
tropics: Ecology, Behavior, Distribution, en-winged Sunbird. Ecology 56:333–45.
and Conservation, ed. A. Keast and E. S. Gill, R. E., T. L. Tibbitts, D. C. Doug-
Morton, pp. 67–78. Washington, DC: las, C. M. Handel, D. M. Mulcahy,
Smithsonian Institution Press. J. C. Gottschalck, N. Warnock, B.
Fleischer, R. C., H. F. James, and S. L. J. McCaffery, P. F. Battley, and T.
Olson. 2008. Convergent evolution of Piersma. 2009. Extreme endurance
Hawaiian and Australo-Pacific honey­ flights by landbirds crossing the Pacific
eaters from distant songbird ancestors. Ocean: Ecological corridor rather than
Current Biology 18:1927–31. barrier? Proceedings of the Royal Society
Flightless bird. All Birds Wiki. allbirdsoft- B 276:447–58.
heworld.wikia.com/​wiki/​flightless_​ Goss-Custard, J. D. 1977. Optimal foraging
bird. and the size selection of worms by red-
Foster, R. B. 1982. The seasonal rhythm shank Tringa tetanus. Animal Behaviour
of fruitfall on Barro Colorado Island. 25:10–29.
In The Ecology of a Tropical Forest, ed. Grant, K. A., and V. Grant. 1968. Hum-
E. G. Leigh Jr., A. S. Rand, and D. M. mingbirds and Their Flowers. New York:
Windsor, pp. 151–72. Washington, DC: Columbia University Press.
Smithsonian Institution Press. Grant, P. R. 1975. The classical case of char-
Foth, C., H. Tischlinger, and O. W. M. acter displacement. Evolutionary Biology
Rauhut. 2014. New specimen of 8:237–337.
Bibliography

Archaeopteryx provides insights into ———. 1985. Climatic fluctuations on the

the evolution of pennaceous feathers. Galapagos Islands and their influence
Nature 511:79. on Darwin’s Finches. In Neotropical
Fretwell, S. 1980. Evolution of migration Ornithology, Ornithological Mono-
in relation to factors regulating bird graphs 36, ed. P. A. Buckley, M. S.

419

1stPages_B.indd 419 7/22/20 11:59 AM

 Foster, E. S. Morton, R. S. Ridgely, and Life-Size Guide to the Eggs of Six Hun-
F. G. Buckley, pp. 471–83. Washington dred of the World’s Bird Species. Chicago:
DC: American Ornithologists’ Union. University of Chicago Press.
Grasse, P. P. 1950. Traite de zoologie. Vol. 15, Hays, H. 1972. Polyandry in the Spotted
Oiseaux. Paris: Masson. Sandpiper. Living Bird 11:43–57.
Greenberg, R., and P. P. Marra, eds. 2005. Hecht, M. K., J. H. Ostrum, G. Viohl, and
Birds of Two Worlds. Baltimore: Johns P. Wellnhofer, eds. 1985. The Begin-
Hopkins University Press. nings of Birds. Eichstätt, Germany:
Grundel, R. 1987. Determinants of nestling Friends of the Jura Museum.
feeding rates and parental investment Heilman, G. 1927. The Origin of Birds. New
in the Mountain Chickadee. Condor York: D. Appleton.
89:319–28. Hertel, F. 1995. Ecomorphological indica-
Hackett, S. J., R. T. Kimball, S. Reddy, R. C. tors of feeding behavior in recent and
K. Bowie, E. L. Braun, M. J. Braun, J. fossil raptors. Auk 112:890–903.
L. Chojnowski, et al. 2008. A phyloge- Hespenheide, H. 1971. Food preferences
netic study of birds reveals their evolu- and the extent of overlap in some insec-
tionary history. Science 320:1763–68. tivorous birds with special reference to
Haffer, J. 1969. Speciation in Amazonian the Tyrannidae. Ibis 113:59–72.
forest birds. Science 165:131–37. Hobson, K. A., S. L. Van Wilgenburg,
Hagan, J. M., III, and D. W. Johnston, eds. J. Faaborg, J. D. Toms, C. Rengifo,
1992. Ecology and Conservation of Neo- A. Llanes Sosa, Y. Aubry, and R.
tropical Migrant Landbirds. Washington, Brito-Aguilar. 2014. Connecting
DC: Smithsonian Institution Press. breeding and wintering grounds of
Hamilton, W. J., III, and F. H. Heppner. Neotropical migrant songbirds using
1967. Radiant solar energy and the stable hydrogen isotopes: A call for an
function of black homeotherm pig- isotopic atlas of migratory connectivity.
mentation: An hypothesis. Science Journal of Field Ornithology 85:237–57.
155:196–97. Holden, C. 2008. Who ate whom? Science
Hamner, W. M. 1963. Diurnal rhythm and 321:1023.
photoperiodism in testicular recru- Holmes, R. T., R. E. Bonney Jr., and S. W.
descence of the House Finch. Science Pacala. 1979. Guild structure of the
142:1294–95. ­Hubbard Brook bird community: A
Hanson, H. C. 2006. The White-Cheeked ­multivariate approach. Ecology 60:512–
Geese: Branta canadensis, B. maxima, 20.
B. ‘lawrensis’, B. hutchinsii, B. leu- Holmes, R. T., and H. F. Recher. 1986.
copareia, and B. minima. Taxonomy, Determinants of guild structure in
Ecophysiographic Relationships, Biogeog- forest bird communities: An interconti-
raphy, and Evolutionary Considerations. nental comparison. Condor 88:427–39.
Vol. 1, Eastern Taxa. Blythe, CA: Avvar Holmes, R. T., and F. W. Sturges. 1975. Bird
Books. community dynamics and energetics
———. 2007. The White-Cheeked Geese: in a northern hardwoods ecosystem.
Branta canadensis, B. maxima, B. ‘law- Journal of Animal Ecology 44:175–200.
rensis’, B. hutchinsii, B. leucopareia, Honovich, N. 2014. The Field Guide to Dino-
Bibliography

and B. minima. Taxonomy, Ecophys- saurs. San Diego, CA: Silver Dolphin
iographic Relationships, Biogeography, Books.
and Evolutionary Considerations. Vol. 2, Houston, A. I., and N. B. Davies. 1985.
Western Taxa. Blythe, CA: Avvar Books. The evolution of cooperation and life
Hauber, M. E. 2014. The Book of Eggs: A history in the Dunnock, Prunella modu-

420

1stPages_B.indd 420 7/22/20 11:59 AM

 laris. In Behavioural Ecology: Ecological James, F. C., and C. E. McCulloch. 1985.
Consequences of Adaptive Behaviour, Data analysis and the design of
ed. R. M. Sibly and R. H. Smith, pp. experiments in ornithology. In Current
471–87. Oxford, England: Blackwell. Ornithology, vol. 2, ed. R. F. Johnston,
Howe, H. F. 1976. Egg size, hatching asyn- pp. 1–63. New York: Plenum.
chrony, sex and brood reduction in the James, F. C., and J. A. Pourtless. 2009. Cla-
Common Grackle. Ecology 57:1195–207. distics and the origin of birds: A review
Howell, S. N. G., and P. Pyle. 2015. Use of and two new analyses. Ornithological
“definitive” and other terms in molt Monographs 66:1–78.
nomenclature: A response to Wolfe et James, H. F., and S. L. Olson. 1983. Flight-
al. (2014). Auk 132:365–69. less birds. Natural History 92:30–40.
Huey, R. B., and C. Deutsch. 2016. How ———. 2004. Fossil birds from the Hawai-
frigate birds soar around the doldrums. ian Islands: Evidence for wholesale
Science 353:26–27. extinction by man before western
Hutchinson, G. E. 1959. Homage to Santa contact. Science 217:633–35.
Rosalia, or why are there so many Jarvis, E. D., S. Mirarab, A. J. Aberer, B.
kinds of animals? American Naturalist Li, P. Houde, C. Li, S. Y. W. Ho, et al.
93:245–49. 2014. Whole-genome analyses resolve
Hutto, R. L. 1994. The composition and early branches in the tree of life of
social organization of mixed-species modern birds. Science 346:1320–31.
flocks in a tropical deciduous forest in Jenni, D. A. 1974. The evolution of poly-
western Mexico. Condor 96:106–16. andry in birds. American Zoologist
Huxley, T. H. 1867. On the classification 142:129–44.
of birds: And on the taxonomic value Johansen, K., and R. W. Millard. 1973.
of the modifications of certain of the Vascular responses to temperature in
cranial bones observable in the class. the foot of the giant fulmar, M­ acronectes
Proceedings of the Zoological Society of giganteus. Journal of Comparative
London 1867:415–72. ­Physiology 85:47–65.
IUCN Red List of Threatened Species. Johnsgard, P. A. 1983. The Hummingbirds
International Union for Conservation of North America. Washington, DC:
of Nature. www.iucnredlist.org. Smithsonian Institution Press.
Jackson, J. A. 1977. Alleviating problems of Johnson, M. D., J. L. Kellerman, and A. M.
competition, predation, parasitism, and Stercho. 2010. Pest reduction services
disease in endangered birds. In Endan- by birds in shade and sun coffee in
gered Birds: Management Techniques for Jamaica. Animal Conservation 13:140–
Preserving Threatened Species, ed. S. A. 47.
Temple, pp. 75–84. Madison: Univer- Johnson, M. J., C. van Riper III, and K. M.
sity of Wisconsin Press. Pearson. 2002. Black-throated Sparrow
Jahn, A. E., V. R. Cueto, J. W. Fox, M. S. (Amphispiza bilineata), version 2.0. In
Husak, D. H. Kim, D. V. Landoll, J. P. The Birds of North America, ed. P. G.
Ledezma, et al. 2013. Migration timing Rodewald. Ithaca, NY: Cornell Lab of
and wintering areas of three species of Ornithology.
flycatchers (Tyrannus) breeding in the Johnston, R. F., and R. C. Fleischer. 1981.
Bibliography

Great Plains of North America. Auk Over-winter mortality and sexual size
130:247–57. dimorphism in the House Sparrow.
James, F. C. 1970. Geographic size varia- Auk 98:503–11.
tion in birds and its relation to climate. Kamil, A. C., and R. P. Balda. 1985. Cache
Ecology 51:365–90. recovery and spatial memory of Clark’s

421

1stPages_B.indd 421 7/22/20 11:59 AM

 Nutcracker (Nucifraga columbiana). key hens. Reproduction 123:79–86.
Journal of Experimental Psychology Kirk, D. A., and M. J. Mossman. 1998. Tur-
11:95–111. key Vulture (Cathartes aura), version
Karr, J. R. 1976. On the relative abundance 2.0. In The Birds of North America, ed.
of migrants from the North Temperate P. G. Rodewald. Ithaca, NY: Cornell
Zone in tropical habitats. Wilson Bulle- Lab of Ornithology.
tin 88:433–58. Klicka, J., A. J. Fry, R. M. Zink, and C. W.
Keast, A. 1980. Spatial relationships Thompson. 2001. A cytochrome-b per-
between migratory parulid warblers spective on Passerina bunting relation-
and their ecological counterparts in the ships. Auk 118:610–23.
Neotropics. In Migrant Birds in the Neo- Kluijver, H. N. 1950. Daily routines of
tropics: Ecology, Behavior, Distribution, the Great Tit, Parus m. major. Ardea
and Conservation, ed. A. Keast and E. S. 38:99–135.
Morton, pp. 109–32. Washington, DC: Konishi, M. 1969. Time resolution by sin-
Smithsonian Institution Press. gle auditory neurons in birds. Nature
Keast, A., and E. S. Morton, eds. 1980. 222:566–67.
Migrant Birds in the Neotropics: Ecology, ———. 1973. How the owl tracks its prey.
Behavior, Distribution, and Conservation. American Scientist 61:414–24.
Washington, DC: Smithsonian Institu- Krebs, J. R. 1977. Song and territory in the
tion Press. Great Tit. In Evolutionary Ecology, ed.
Keeton, W. T. 1969. Orientation by pigeons: B. Stonehouse and C. M. Perrins, pp.
Is the sun necessary? Science 165:922– 47–62. London: Macmillan.
28. Krebs, J. R., and M. I. Avery. 1985. Central
———. 1974. The mystery of pigeon place foraging in the European Bee-
­homing. Scientific American 23:96–107. eater, Merops apiaster. Journal of Animal
Kellert, S. R. 1980. Activities of the Ameri- Ecology 54:459–72.
can Public Relating to Animals. Phase II Krebs, J. R., D. W. Stephens, and W. J.
Report. Washington, DC: US Depart- Sutherland. 1977. Perspectives in
ment of the Interior, Fish and Wildlife optimal foraging. In Perspectives in
Service. Ornithology, ed. A. H. Brush and G.
Kendeigh, S. C. 1961. Energy of birds con- A. Clark Jr., pp. 165–216. Cambridge:
served by roosting in cavities. Wilson Cambridge University Press.
Bulletin 73:140–47. Kroodsma, D. E. 1982. Song repertoires:
Kendeigh, S. C., V. R. Dol’nik, and V. M. Problems in their definition and use.
Gavrilkov. 1977. Avian energetics. In In Acoustic Communication in Birds, vol.
Granivorous Birds in Ecosystems, ed. 2, ed. D. E. Kroodsma and E. H. Miller,
J. Pinkowski and S. C. Kendeigh, pp. pp. 125–46. New York: Academic Press.
127–204. Cambridge: Cambridge Uni- ———. 1985. Geographic variation in
versity Press. songs of the Bewick’s wren: A search
Ketterson, E. D., and V. Nolan Jr. 1976. for correlations with avifaunal complex-
Geographic variation and its climatic ity. Behavioral Ecology and Sociobiology
correlates in the sex ratio of east- 16:143–50.
ern-wintering Dark-eyed Juncos (Junco ———. 1986. The spice of bird song. Living
Bibliography

hyemalis hyemalis). Ecology 57:679–93. Bird Quarterly 5:12–16.

King, L. M., J. P. Buillard, W. M. Garrett, Kroodsma, R. L. 1975. Hybridization in
M. R. Bakst, and A. M. Donoghue. buntings (Passerina) in North Dakota
2002. Segregation of spermatozoa with and eastern Montana. Auk 92:66–80.
sperm storage tubules of fowl and tur- Ksepka, D. 2014. Flight performance of the

422

1stPages_B.indd 422 7/22/20 11:59 AM

 largest volant bird. Proceedings of the doba-Córdoba, M. Echeverry-Galvis, et
National Academy of Sciences 111:10624– al. 2010. A comprehensive multilocus
29. phylogeny for the wood-warblers and
Lack, D. 1963. Cuckoo hosts in England. a revised classification of the Parulidae
With an appendix on the cuckoo hosts (Aves). Molecular Phylogenetics and
of Japan, by T. Royama. Bird Study Evolution 57:753–70.
10:185–203. Lucas, A. M., and P. R. Stettenheim. 1972.
———. 1968. Ecological Adaptations for Avian Anatomy: Integument. 2 vols. Agri-
Breeding in Birds. London: Methuen. culture Handbook No. 3652. Wash-
———. 1971. Ecological Isolation in Birds. ington, DC: US Government Printing
Oxford, England: Blackwell. Office.
Lasiewski, R. C. 1963. Oxygen consump- Lustick, S., M. Adam, and A. Hinko. 1980.
tion of torpid, resting, active, and flying Interaction between posture, color,
hummingbirds. Physiological Zoology and radiative heat load in birds. Science
36:122–40. 208:1052–53.
———. 1969. Physiological responses to MacArthur, R. H. 1958. Population ecology
heat stress in the Poorwill. American of some warblers of northeastern conif-
Journal of Physiology 217:1504–9. erous forests. Ecology 39:599–619.
Lawler, Andrew. 2014. Why Did the Chicken ———. 1959. On the breeding distribution
Cross the World? The Epic Saga of the patterns of North American migrant
Bird that Powers Civilization. New York: birds. Auk 76:318–25.
Atria Books ———. 1972. Geographical Ecology. New
Lein, M. R. 1972. A trophic comparison of York: Harper and Row.
avifaunas. Systematic Zoology 21:135–50. MacArthur, R. H., and E. O. Wilson. 1963.
Ligon, J. D., and S. H. Ligon. 1978. The An equilibrium theory of insular zoo-
communal social system of the Green geography. Evolution 17:373–87.
Woodhoopoe in Kenya. Living Bird ———. 1967. The Theory of Island Bio­
17:159–97. geography. Princeton, NJ: Princeton
———. 1982. The cooperative breeding University Press.
behavior of the Green Woodhoopoe. Marten, J. A., and N. K. Johnson. 1986.
Scientific American 247:126–34. Genetic relationships of North Amer-
Lill, A. 1974. Sexual behavior of the ican cardueline finches. Condor
lek-forming White-bearded Manakin 88:409–20.
(Manacus m. trinitatis Harterat). Marzluff, J. M., J. Walls, H. N. Cornell, J. C.
Zeitschrift für Tierpsychologie 36:1–36. Withey, and D. P. Craig. 2010. Last-
Livezey, B. C., and R. L. Zusi. 2007. High- ing recognition of threatening people
er-order phylogeny of modern birds by wild American Crows. Animal
(Theropoda, Aves: Neornithes) based Behaviour 79:699–707.
on comparative anatomy. II. Analysis Mazzeo, R. 1953. Homing of the Manx
and discussion. Zoological Journal of the Shearwater. Auk 70:200–201.
Linnean Society 149:1–95. McCracken, K. G. 2000. The 20-cm spiny
Logan, C. J., S. A. Jelbert, A. J. Breen, R. D. penis of the Argentine Lake Duck (Oxy-
Gray, and A. H. Taylor. 2014. Modifi- ura vittata). Auk 117:820–25.
Bibliography

cations to the Aesop’s fable paradigm McGillivray, W. E. 1983. Intraseasonal

change New Caledonian Crow perfor- reproductive costs for the House Spar-
mances. PLoS ONE 9:e103049. row (Passer domesticus). Auk 100:25–32.
Lovette, I. J., J. L. Pérez-Emán, J. P. Sulli- McKinnon, E. A., K. C. Fraser, and B. J. M.
van, R. C. Banks, I. Fiorentino, S. Cór- Stutchbury. 2013. New discoveries in

423

1stPages_B.indd 423 7/22/20 11:59 AM

 landbird migration using geolocators, ———. 2013. Into the minds of birds. Sci-
and a flight plan for the future. Auk ence 341:22–25.
130:211–22. ———. 2015. A bit of altruism makes
McKitrick, M. C., and R. M. Zink. 1988. V-shaped flocks of birds possible. Sci-
Species concepts in ornithology. Condor ence. doi:10.1126/​science.aaa7789.
90:1–14. Morton, E. S. 1970. Ecological sources of
Meier, A. H., and B. R. Ferrell. 1978. Avian selection on avian sound. PhD diss.,
endocrinology. In Chemical Zoology, ed. Yale University, New Haven, CT.
M. Florkin, B. Scheer, and J. Brush, pp. Morton, M. L., and C. Carey. 1971. Growth
213–71. New York: Academic Press. and development of endothermy in
Mengel, R. M. 1964. The probable history Mountain White-crowned Sparrows
of species formation in some northern (Zonotrichia leucophrys oriantha). Physi-
wood warblers (Parulidae). Living Bird ological Zoology 44:177–89.
3:9–43. Mugaas, J. N., and J. R. King. 1981. Annual
Mewaldt, L. R. 1958. Pterylography and Variation of Daily Energy Expenditure by
natural and experimentally induced the Black-billed Magpie. Studies in Avian
molt in Clark’s Nutcracker. Condor Biology, no. 5. Columbus, OH: Cooper
60:165–87. Ornithological Society.
Mihailova, M., M. L. Berg, K. L. Buchanan, Munn, C. A. 1985. Permanent canopy and
and A. T. D. Bennett. 2014. Odour- understory flocks in Amazonia: Species
based discrimination of subspecies, composition and population density. In
species and sexes in an avian species Neotropical Ornithology, Ornithological
complex, the Crimson Rosella. Animal Monographs 36, ed. P. A. Buckley, M.
Behaviour 95:155–64. S. Foster, E. S. Morton, R. S. Ridgely,
Millener, P. R. 1989. The only flightless and P. G. Buckley, pp. 683–712. Wash-
passerine: The Stephens Island Wren ington, DC: American Ornithologists’
(Traversia lyalli: Acanthisittidae). Notor- Union.
nis 36:280–84. Murton, R. K., and N. J. Westwood. 1977.
Millennium Ecosystem Assessment. 2005. Avian Breeding Cycles. Oxford, England:
Ecosystems and Human Well-Being: Syn- Clarendon Press.
thesis. Washington, DC: Island Press. Myers, J. P. 1980. The pampas shorebird
Mlikovsky, J. 2003. Eggs of extinct aepyor- community: Interactions between
nithids (Aves: Aepyornithidae) of Mad- breeding and non-breeding members.
agascar: Size and taxonomic identity. In Migrant Birds in the Neotropics: Ecol-
Sylvia 39:133–38. ogy, Behavior, Distribution, and Conser-
Moreau, R. E. 1972. The Palearctic-African vation, ed. A. Keast and E. S. Morton,
Bird Migration Systems. New York: Aca- pp. 37–50. Washington, DC: Smithso-
demic Press. nian Institution Press.
Morel, M.-Y. 1973. Contribution a l’étude Nakane, Y., T. Shimmura, H. Abe, and T.
dynamique de la population de Lag- Yoshimura. 2014. Intrinsic photosen-
onostica senegala L. (estrildides) à Rich- sitivity of a deep brain photoreceptor.
ard-Toll (Sénégal). Interelations avec le Current Biology 24(13):R596–R597.
parasite Hypochera chalybeata (Müller) Nottebohm, F. 1975. Continental patterns
Bibliography

(viduines). Mémoires du Muséum of song variability in Zonotrichia capen-

National d’Histoire Naturelle, Sér. A. sis: Some possible ecological correlates.
Zoologie 78:1–156. American Naturalist 109:605–24.
Morrell, V. 2011. No Joke: Pigeons ace a sim- O’Connor, R. J. 1984. The Growth and Develop-
ple math test. Science, December 22. ment of Birds. New York: Wiley and Sons.

424

1stPages_B.indd 424 7/22/20 11:59 AM

 Ohmart, R. D., and R. C. Lasiewski. 1971. the beginning of the embryonic circula-
Roadrunners: Energy conservation by tion. American Scientist 39:225–43.
hypothermia and absorption of sun- Payne, R. B. 1977. The ecology of brood
light. Science 172:67–69. parasitism in birds. Annual Review of
Olson, S. L., and J. W. Wiley. 2016. The Ecology and Systematics 8:1–28.
Blue-headed Quail-dove (Starnoenas PBS. 2005. Bird brain. Science Now.
cyanocephala): An Australasian dove NOVA. http://​www.pbs.org/​wgbh/​
marooned in Cuba. Wilson Journal of nova/​sciencenow/​3214/​03-brain.html.
Ornithology 128(1):1–21. Pennisi, E. 2014. Bird genomes give
Oniki, Y. 1985. Why robin eggs are blue and new perches to old friends. Science
birds build nests: Statistical tests for 346:1275–76.
Amazonian birds. In Neotropical Orni- Pennycuick, C. J. 1975. Mechanics of flight.
thology, Ornithological Monographs In Avian Biology, vol. 5, ed. D. S. Farner
36, ed. P. A. Buckley, M. S. Foster, R. S. and J. R. King, pp. 1–75. New York:
Ridgely, and F. G. Buckley, pp. 536–45. Academic Press.
Washington, DC: American Ornitholo- Perdeck, A. C. 1958. Two types of orien-
gists’ Union. tation in migrating Starlings Sturnus
Orians, G. H. 1969. On the evolution of vulgaris L., and Chaffinches Fringilla
mating systems by birds and mam- coelebs L., as revealed by displacement
mals. American Naturalist 103:589–603. experiments. Ardea 46:1–37.
Orians, G. H., and G. M. Christman. 1968. Perkins, S. 2015. New species of “terror
A comparative study of the behavior bird” discovered. Science. doi:10.1126/​
of Red-winged, Tricolored, and Yel- science.aab2465.
low-headed Blackbirds. University Perrins, C. M. 1964. Survival of young
of California Publications in Zoology swifts in relation to brood size. Nature
84:1–85. 201:1147–48.
Orians, G. H., and M. F. Willson. 1964. ———. 1965. Population fluctuations and
Interspecific territories of birds. Ecology clutch size in the Great Tit, Parus major
45:736–45. L. Journal of Animal Ecology 34:601–47.
Oring, L. W. 1986. Avian polyandry: A ———. 1976. Possible effects of qualitative
review. In Current Ornithology, vol. 3, changes in the insect diet of an avian
ed. R. F. Johnston, pp. 309–51. New predator. Ibis 118:580–84.
York: Plenum. ———. 1980. Survival of young Great Tits,
Ortega, C. R., A. Cruz, and M. E. Mermoz. Parus major. Acta Congressus Interna-
2005. Issues and controversies of Cow- tionalus Ornithologici 2:159–74.
bird (Molothrus) management. Ornitho- Perrins, C. M., and T. R. Birkhead. 1983.
logical Monographs 57:6–15. Avian Ecology. Glasgow, Scotland:
Ostrum, J. H. 1979. Bird flight: How did it Blackie and Sons.
begin? American Scientist 67:46–56. Perrins, C. M., and D. Moss. 1975. Repro-
Page, G., and D. F. Whitacre. 1975. Raptor ductive rates of the Great Tit. Journal of
predation on wintering shorebirds. Animal Ecology 44:695–706.
Condor 77:73–83. Peters, J. L. 1979. Check-list of Birds of the
Parker, P. G., and N. T. Burley, eds. 1998. World, vol. 1. Revision of the work of J.
Bibliography

Avian Reproductive Tactics: Female and L. Peters, E. Mayr, and G. W. Cottrell,

Male Perspectives. Ornithological Mono- eds. Cambridge, MA: Museum of Com-
graphs 49. Washington, DC: American parative Zoology.
Ornithologists’ Union. Petren, K., B. R. Grant, and P. R. Grant.
Patten, B. M. 1951. The first heart beats and 1999. A phylogeny of Darwin’s finches

425

1stPages_B.indd 425 7/22/20 11:59 AM

 based on microsatellite DNA length ine Birds (Acanthisittidae, Pittidae,
variation. Proceedings of the Royal Society Philepittidae, Eurylaimidae). Ornitho-
B 266:321–30. logical Monographs 41. Washington,
Phillips, J. C., P. J. Butler, and P. J. Sharp. DC: American Ornithologists’ Union.
1985. Physiological Strategies in Avian Ralph, C. J., and C. van Riper III. 1985.
Biology. Glasgow, Scotland: Blackie and Historical and current factors affecting
Son. Hawaiian native birds. Bird Conserva-
Pitcher, T. E., P. O. Dunn, and L. A. Whit- tion 2:7–42.
tingham. 2005. Sperm competition Rappole, J. H., E. S. Morton, T. E. Lovejoy,
and the evolution of testes size in and J. L. Ruos. 1983. Nearctic Avian
birds. Journal of Evolutionary Biology Migrants in the Neotropics. Washington,
18:557–67. DC: US Department of the Interior,
Pitelka, F. A., R. T. Holmes, and S. F. Fish and Wildlife Service.
MacLean Jr. 1964. Ecology and evo- Regal, P. J. 1975. The evolutionary origin
lution of social organization in Arctic of feathers. Quarterly Review of Biology
sandpipers. American Zoologist 14:185– 50:35–66.
204. Rice, J. 1978a. Behavioural interactions of
Prum, R. O. 2002. Why ornithologists interspecifically territorial vireos. I.
should care about the theropod origin Song discrimination and natural inter-
of birds. Auk 119:1–17. actions. Animal Behaviour 26:527–49.
———. 2003. Are current critiques of ———. 1978b. Ecological relationships of
the theropod origin of birds science? two interspecifically territorial vireos.
Rebuttal to Feduccia (2002). Auk Ecology 59:526–38.
120:550–61. Ricklefs, R. E. 1969. Adaptation, constraint,
Prum, R. O., K. S. Berv, A. Dornburg, D. J. and compromise in avian postnatal
Field, J. P. Townsend, E. M. Lemmon, development. Biological Review 54:269–
and A. R. Lemmon. 2015. A compre- 90.
hensive phylogeny of birds (Aves) ———. 1980. Geographical variations in
using targeted next-generation DNA clutch-size among passerine birds:
sequencing. Nature 526:569–77. Ashmole’s hypothesis. Auk 97:38–49.
Pulliam, H. R., K. A. Anderson, A. Misztal, ———. 1983. Postnatal development. In
and N. Moore. 1974. Temperature-de- Avian Biology, vol. 7, ed. D. S. Farner,
pendent social behavior in juncos. Ibis J. R. King, and K. C. Parkes, pp. 1–83.
116:360–64. New York: Academic Press.
Quick, D. E., and J. A. Ruben. 2009. Car- Ricklefs, R. E., and G. W. Cox. 1972. Taxon
dio-pulmonary anatomy in theropod cycles in the West Indian avifauna.
dinosaurs: Implications from extant American Naturalist 106:195–219.
archosaurs. Journal of Morphology Ridpath, M. G. 1972. The Tasmanian native
270:1232–46. hen, Tribonyx mortierii. I. Patterns
Rahn, H., and A. Ar. 1974. The avian egg: of behavior. CSIRO Wildlife Research
Incubation time and water loss. Condor 17:1–51.
76:147–52. Robbins, M. V., J. Braun, and E. A. Tobey.
Raikow, R. J. 1985. Problems in avian clas- 1986. Morphological and vocal varia-
Bibliography

sification. In Current Ornithology, vol. tion across a contact zone between the
2, ed. R. F. Johnston, pp. 187–212. New chickadees Parus atricapillus and P.
York: Plenum. carolinensis. Auk 103:655–66.
———. 1987. Hindlimb Myology and Evolu- Robinson, S. K., and R. T. Holmes. 1982.
tion of the Old World Suboscine Passer- Foraging behavior of forest birds: The

426

1stPages_B.indd 426 7/22/20 11:59 AM

 relationships among search tactics, competition in the Aquatic Warbler
diet, and habitat structure. Ecology Acrocephalus paludicola. Ibis 137:85–91.
63:1918–31. Sereno, P. C. 1999. The evolution of dino-
Rodgers, P. 2009. Maori legend of saurs. Science 284:2137–47.
man-eating bird is true. Independent. Shefte, N., R. L. Bruggers, and E. W. Scha-
https://www.independent.co.uk/envi- fer Jr. 1982. Repellency and toxicity
ronment/nature/maori-legend-of-man- of three bird control chemicals to
eating-bird-is-true-1786867.html. four species of African grain-eating
Rohwer, S. A. 1975. The social significance birds. Journal of Wildlife Management
of avian winter plumage variability. 46:453–57.
Evolution 29:593–610. Sherry, T. W., and R. T. Holmes. 1992. Pop-
Rohwer, S. A., and G. S. Butcher. 1988. ulation fluctuations in a long-distance
Winter versus summer explanations Neotropical migrant: Demographic
of delayed plumage maturation in evidence for the importance of breeding
temperate passerine birds. American season events in the American Redstart.
Naturalist 131:556–72. In Ecology and Conservation of Neotropi-
Romanoff, A. L., and A. J. Romanoff. 1949. cal Migrant Landbirds, ed. J. M. Hagan
The Avian Egg. New York: Wiley. III and D. W. Johnston, pp. 431–42.
Ruppell, W. 1944. Versuche über Heim- Washington, DC: Smithsonian Institu-
finden ziehender Nebalkrähen nach tion Press.
Verfrachtung. Journal für Ornithologie Sibley, C. G. 1973. The relationships of the
92:106–33. silky flycatchers. Auk 90:394–410.
Russell, S. M. 1969. Regulation of egg tem- Sibley, C. G., and J. E. Ahlquist. 1983. Phy-
perature by incubating White-winged logeny and classification of birds based
Doves. In Physiological Systems in Semi- on the data of DNA-DNA hybridization.
Arid Environments, ed. C. C. Hoff and In Current Ornithology, vol. 1, ed. R.
M. L. Riedesel, pp. 107–12. Albuquer- F. Johnston, pp. 245–92. New York:
que: University of New Mexico Press. Plenum.
Sanderson, J. G., J. Diamond, and S. L. ———. 1990. Phylogeny and Classification
Pimm. 2011. Response to Collins et al. of Birds: A Study in Molecular Evolution.
(2011). Journal of Biogeography 38:2397– New Haven, CT: Yale University Press.
404. Sibley, C. G., and B. L. Monroe Jr. 1990.
Savile, D. B. O. 1957. Adaptive evolution in Distribution and Taxonomy of Birds of
the avian wing. Evolution 11:212–24. the World. New Haven, CT: Yale Univer-
Schmidt-Nielsen, K. 1959. Salt glands. sity Press.
Scientific American 200:109–16. Silcock, F. 2006. A review of accounts of
Schnell, F. D. 1970. A phenetic study of the luminosity in Barn Owls Tyto alba. The
suborder Lari (Aves). II. Phenograms, Owl Pages. http://​www.owlpages.com/​
discussion, and conclusions. Systematic articles.php?section=Studies+and+Pa-
Zoology 19:264–302. pers&title=Min+Min.
Schoener, T. W. 1968. Sizes of feeding terri- Simberloff, D. S., and W. Boecklen. 1981.
tories among birds. Ecology 49:123–41. Santa Rosalia reconsidered: Size ratios
———. 1983. Field experiments on inter- and competition. Evolution 35:1206–28.
Bibliography

specific competition. American Natural- Skaudhage, E. 1981. Osmoregulation in

ist 30:240–85. Birds. Berlin: Springer-Verlag.
Schulze-Hagen, K., B. Leilser, T. R. Birk- Smith, N. A., L. M. Chiappe, J. A. Clarke, S.
head, and A. Dyrcz. 1995. Prolonged V. Edwards, S. J. Nesbitt, M. A. Norell,
copulation, sperm reserves and sperm T. A. Stidham, et al. 2015. Rhetoric

427

1stPages_B.indd 427 7/22/20 11:59 AM

 vs. reality: A commentary on “Bird ———. 1980. The conservation status of
Origins Anew” by A. Feduccia. Auk Neotropical migrants: Present and
132:467–80. future. In Migrant Birds in the Neo-
Snow, D. W. 1964. A possible selective fac- tropics: Ecology, Behavior, Distribution,
tor in the evolution of fruiting seasons and Conservation, ed. A. Keast and E. S.
in tropical forest. Oikos 15:274–81. Morton, pp. 21–30. Washington, DC:
Sossinka, R. 1982. Domestication in birds. Smithsonian Institution Press.
In Avian Biology, vol. 6, ed. D. S. ———. 1985. The role of ecotones in the
Farner, J. R. King, and K. C. Parkes, pp. distribution of Andean birds. Ecology
373–403. New York: Academic Press. 66:1237–46.
Sotherland, P. R., and H. Rahn. 1987. On Terborgh, J., and J. Faaborg. 1973. Turnover
the composition of bird eggs. Condor and ecological release in the birds of
89:48–65. Mona Island, Puerto Rico. Auk 90:759–
Stacey, P. B., and W. D. Koenig. 1984. 79.
Cooperative breeding in the Acorn ———. 1980. Saturation of bird commu-
Woodpecker. Scientific American nities in the West Indies. American
251:114–21. Naturalist 116:178–95.
Stalmaster, M. V., and J. A. Gessaman. Terborgh, J., and J. S. Weske. 1975. The role
1984. Ecological energetics and of competition in the distribution of
foraging behavior of overwintering Andean birds. Ecology 56:562–76.
Bald Eagles. Ecological Monographs Thiollay, J.-M., and M. Jullien. 1998. Flock-
54:407–28. ing behavior of foraging birds in a Neo-
Steadman, D. W. 1982. The origin of tropical rainforest and the antipredator
Darwin’s finches (Fringillidae, Passer- defence hypothesis. Ibis 140:382–94.
iformes). Transactions of the San Diego Thomas, D. H. 1982. Salt and water excre-
Society of Natural History 19:279–96. tion by birds: The lower intestine as
Stenger, J. 1958. Food habits and available an integrator of renal and intestinal
food of ovenbirds in relation to territory excretion. Comparative Biochemistry and
size. Auk 75:335–46. Physiology 71A:527–36.
Stiles, F. G. 1982. Aggressive and courtship Thomas, G. H. 2015. An avian explosion.
displays of the male Anna’s Humming- Nature 526:516–17.
bird. Condor 84:208–25. Thorpe, W. H. 1961. Bird Song: The Biology
Street prophets coffee hour: Bird super of Vocal Communication and Expression
vision. 2013. Daily Kos. http://​www. in Birds. Cambridge: Cambridge Uni-
dailykos.com/​story/​2013/​06/​17/​ versity Press.
1216709/-Street-Prophets-Coffee-Hour- Tinbergen, J. M. 1981. Foraging decisions
Bird-Super-Vision#. in starlings (Sturnus vulgaris L.). Ardea
Stutchbury, B. J. M., and E. S. Mor- 69:1–67.
ton. 2008. Recent advances in the Tinbergen, N. 1951. The Study of Instinct.
behavioural ecology of tropical birds. Oxford, England: Clarendon Press.
Wilson Journal of Ornithology 120:26– Tucker, V. A. 1968. Respiratory physiology
37. of House Sparrows in relation to high
Terborgh, J. 1971. Distribution on environ- altitude flight. Journal of Experimental
Bibliography

mental gradients: Theory and a prelimi- Biology 48:617–33.

nary interpretation of distributional pat- Turcek, F. J. 1966. On plumage quantity in
terns in the avifauna of the Cordillera birds. Ekologia Polska Ser. A 14:617–33.
Vilcabamba, Peru. Ecology 32:23–40. University of Montana. 2009. How a new

428

1stPages_B.indd 428 7/22/20 11:59 AM

 theory of bird evolution came about. Wang, M., X. Zheng, J. K. O’Connor, G. T.
ScienceDaily, March 3. Lloyd, X. Wang, Y. Wang, X. Zhang,
USDA (US Department of Agriculture). and Z. Zhou. 2015. The oldest record of
2016. Poultry – production and value: ornithuromorpha from the early Creta-
2015 summary. ISSN 1949-1573. ceous of China. Nature Communications
US Fish and Wildlife Service. 2018a. 6:6987.
Hunting. http://​www.fws.gov/​birds/​ Wantanabe, S. 2010. Pigeons can discrim-
bird-enthusiasts/​hunting.php. inate “good” and “bad” paintings by
———. 2018b. Economic impact: Birds, children. Animal Cognition 12:119–25.
bird watching and the U.S. economy. Weeks, H. P. 1978. Clutch size variation in
http://​www.fws.gov/​birds/​bird-enthusi- the Eastern Phoebe in southern Indi-
asts/​bird-watching/​valuing-birds.php. ana. Auk 95:656–66.
Van Rhijn, J., J. Jukema, and T. Piersma. Weimerskirch, H., C. Bishop, T. Jeanniard-
2014. Diversity of nuptial plumages in du-Dot, A. Prudor, and G. Sachs. 2016.
male Ruffs Philomachus pugnax. Ardea Frigate birds track atmospheric condi-
102:5–20. tions over months-long transoceanic
Van Tyne, J., and A. J. Berger. 1976. Funda- flights. Science 353:74–77.
mentals of Ornithology. New York: John Weller, M. W. 1967. Notes on plumages and
Wiley. weights of the Black-headed Duck Het-
Vehrencamp, S. L. 1977. Relative fecundity eronetta atricapilla. Condor 69:133–45.
and parental effort in communally ———. 1976. Molts and plumages of
nesting anis. Science 197:403–5. waterfowl. In Ducks, Geese, and Swans
Verner, J. 1977. On the adaptive signifi- of North America, ed. F. C. Bellrose,
cance of territoriality. American Natu- pp. 34–38. Harrisburg, PA: Stackpole
ralist 111:769–75. Books.
Verner, J., and M. F. Willson. 1966. The ———. 1980. The Island Waterfowl. Ames:
influence of habitats on mating sys- Iowa State University Press.
tems of North American passerine Welty, J. C. 1955. Birds as flying machines.
birds. Ecology 47:143–47. Scientific American 192:88–96.
Vince, M. A. 1969. Embryonic communica- White, F. N., G. A. Bartholomew, and T. R.
tion, respiration, and the synchroniza- Howell. 1975. The thermal significance
tion of hatching. In Bird Vocalizations, of the nest of the Sociable Weaver
ed. R. A. Hinde, pp. 233–60. Cam- (Philetarus socius): Winter observations.
bridge: Cambridge University Press. Ibis 117:171–79.
von Haartman, L. 1949. Der Trauerfliegen- Whittow, G. C. 1986a. Regulation of body
schnäpper. I. Ortstreue und Rassenbil- temperature. In Avian Physiology, 4th
dung. Acta Zoologica Fennica 56:1–104. ed., ed. P. D. Sturkie, pp. 221–52. New
———. 1969. Nest site and evolution of York: Springer-Verlag.
polygamy in European passerine birds. ———. 1986b. Energy metabolism.
Ornis Fennica 46:1–12. In Avian Physiology, 4th ed., ed. P.
Wagner, H. O. 1954. Versuch einer Analyse D. Sturkie, pp. 253–68. New York:
der Kolibribalz. Zeitschrift für Tierpsy- ­Springer-Verlag.
chologie 11:182–212. Wiens, J. A. 1986. Spatial scale and tempo-
Bibliography

Waldron, P. 2014. Why birds fly in a V ral variation in studies of shrub-steppe

formation. Science. http://​news.science- birds. In Community Ecology, ed. J. R.
mag.org/​biology/​2014/​01/​why-birds- Diamond and R. Case, pp. 154–72. New
fly-v-­formation. York: Harper and Row.

429

1stPages_B.indd 429 7/22/20 11:59 AM

 Wiley, R. H. 1973. Territoriality and Wolfe, J. D., E. K. Johnson, and R. S. Terrill.
non-random mating in the Sage 2014. Searching for consensus in molt
Grouse Centrocercus urophasianus. Ani- terminology 11 years after Howell et
mal Behavior Monographs 6:87–169. al.’s “first basic problem.” Auk 131:371–
Willis, E. O. 1974. Populations and local 77.
extinctions of birds on Barro Colorado Wood, B. J., and C. G. Fee. 2003. A critical
Island, Panama. Ecological Monographs review of the development of rat con-
44:153–69. trol in Malaysian agriculture since the
———. 1980. Ecological roles of migratory 1960s. Crop Protection 22:445–61.
and resident birds on Barro Colorado Woolfenden, G. E., and J. Fitzpatrick.
Island, Panama. In Migrant Birds in the 1978. The importance of territory
Neotropics: Ecology, Behavior, Distribu- in group-breeding birds. BioScience
tion, and Conservation, ed. A. Keast and 28:104–8.
E. S. Morton, pp. 205–26. Washington, ———. 1984. The Florida Scrub Jay:
DC: Smithsonian Institution Press. ­Demography of a Cooperative-Breeding
Willson, M. F. 1976. The breeding distribu- Bird. Princeton, NJ: Princeton Univer-
tion of North American migrant birds: sity Press.
A critique of MacArthur (1959). Wilson Worthy, T. H., and R. P. Scofield. 2012.
Bulletin 88:582–87. Twenty-first century advances in
Wilson, B. W. 1980. Birds: Readings from knowledge of the biology of moa (Aves:
Scientific American. San Francisco: W. Dinornithiformes): A new morphologi-
H. Freeman. cal analysis and moa diagnoses revised.
Wiltschko, W. 1968. Über den Einfluss New Zealand Journal of Zoology 39:87.
statischer Magnetfelder auf die Zugori- Xu, X., Z. Zhou, R. Dudley, S. Mackem,
entierung der Rotkehlchen (Erithacus C.-M. Chuong, G. M. Erickson, and
rubecula). Zeitschrift für Tierpsychologie D. J. Varricchio. 2014. An integrative
25:537–58. approach to understanding bird ori-
———. 1972. The influence of magnetic gins. Science 346:1253293.
field intensity and inclination on direc- Yeaton, R. I., and M. L. Cody. 1974.
tions preferred by migrating European ­Competitive release in island Song
Robins (Erithacus rubecula). ASA ­Sparrow populations. Theoretical
Special Publication NASA SP-262, pp. ­Population ­Biology 5:42–58.
569–78. Zhang, G., C. Li, Q. Li, B. Li, D. M.
Winklhofer, M. 2012. An avian magnetom- ­Larkin, C. Lee, J. F. Storz, et al. 2014.
eter. Science 336:991–92. ­Comparative genomics reveals insights
Withers, P. C. 1977. Respiration, metabo- into avian genome evolution and
lism, and heat exchange of euthermic ­adaptation. Science 346:1311–20.
and torpid poorwills and humming- Zheng, X., Z. Zhou, X. Wang, F. Zhang,
birds. Physiological Zoology 50:43–52. X. Zhang, Y. Wang, G. Wei, S. Wang,
Witschi, E. 1935. Seasonal sex characters and X. Xu. 2013. Hind wings in basal
in birds and their hormonal control. birds and the evolution of leg feathers.
Wilson Bulletin 47:177–88. Science 33:1309–12.
Wolf, L. L., and F. R. Hainsworth. 1972. Zink, R. M. 2002. A new perspective on
Bibliography

Environmental influence on regulated the evolutionary history of Darwin’s

body temperatures in torpid humming- Finches. Auk 119:864–71.
birds. Comparative Biochemistry and
Physiology 41A:167–73.

430

1stPages_B.indd 430 7/22/20 11:59 AM

 SUGGESTED READING

Chapter 1 one might want to know about feathers,

starting with their evolution 100 million
Chambers, P. 2002. Bones of Contention: years ago and ending with the economic
The Archaeopteryx Scandals. London: value of feathers in the modern world.
John Murray. An inside look at the Lazareva, O. F., T. Shimizu, and E. A.
evidence and personalities involved in the Wasserman. 2012. How Animals See the
controversy over the release of Darwin’s World: Comparative Behavior, Biology,
book on evolution and the discovery of and Evolution of Vision. New York:
Archaeopteryx. Oxford University Press. Although
Feduccia, A. 2012. Riddle of the Feathered this is much broader than just birds, it
Dragons: Hidden Birds of China. New includes a great deal of information on
Haven, CT: Yale University Press. An avian vision and how it compares to
expansive examination of the “old school” vision in humans and other animals.
hypotheses of how birds evolved, incorpo-
rating many of the recent discoveries of Chapter 3
fossils from China.
Prum, R. O. 2002. Why ornithologists Hecht, M. K. J. H. Ostrom, G. Viohl, and
should care about the theropod origin P. Wellnhoffer. 1985. The Beginnings
of birds. Auk 119:1–17. This article of Birds. Eichstätt: Friends of the Jura
initiated an exchange of articles between Museum. Although this volume focuses
the new ideas on bird evolution (presented on the role of Archaeopteryx in the evo-
by Prum) and the older ideas (presented lution of birds, it is impossible to separate
by Alan Feduccia). These four papers this discussion from that concerning the
present both the science and sociology of evolution of flight. Thus, selected papers in
science involved in the arguments about this volume focus on the arguments over
avian origins and provide a multitude of the origin and evolution of flight, often
references on this topic. with discussions of the basic components
of flight mechanics.
Chapter 2 James, H. F., and S. L. Olson. 1983. Flight-
less birds. Natural History 92:30–40. A
Birkhead, T. 2012. Bird Sense: What It’s Like focus on the evolution of flightless birds in
to Be a Bird. New York: Walker. This the Hawaiian avifauna.
delightful book attempts to see how birds Pennycuick, C. J. 1975. Mechanics of flight.
view the world and how humans cannot In Avian Biology, vol. 5, ed. D. S. Farner,
always match this view. It starts with the J. R. King, and K. C. Parkes, pp. 1–75.
standard senses (vision, hearing, touch, New York: Academic Press. A very
taste, and smell) and ends with magnetic detailed, often highly mathematical look
senses and emotions. at the mechanics of bird flight. Topics
Hanson, T. 2011. Feathers: The Evolution discussed include powered flight, soaring,
of a Natural Miracle. New York: Basic and gliding and some of the physical and
Books. This book covers nearly everything mechanical limitations to these forms of
flight.

431

1stPages_B.indd 431 7/22/20 11:59 AM

 Ruppell, G. 1977. Bird Flight. New York: Storer, R. W. 1971. Adaptive radiation in
Van Nostrand Reinhold. A detailed birds. In Avian Biology, vol. 1, ed. D.
examination of bird flight. S. Farner and J. R. King, pp. 149–88.
New York: Academic Press. This
Chapter 4 chapter introduces the reader to some of
the constraints on the radiation of birds
Cracraft, J. 1983. Species concepts and and the variation that has occurred
speciation analysis. Current Ornithology during avian evolution. Included are brief
1:159–87. This article discusses many of reviews of locomotory adaptations, adap-
the problems associated with the biological tations for feeding, and some examples of
species concept and classical speciation adaptive radiations within groups.
analysis. To the extent that the previous Wiens, J. A., ed. 1982. Forum: Avian sub-
reading reflects the history of speciation species in the 1980’s. Auk 99:593–614.
studies in birds, this article suggests possi- This is a selection of short commentaries
ble future directions. by 11 different ornithologists discussing
Diamond, J. M. 1979. Niche shifts and the both the strengths and weaknesses of the
rediscovery of interspecific competi- subspecies concept in avian studies.
tion. American Scientist 66:322–31. This
popular article reviews the controversy Chapter 5
over the role of interspecific competition
in affecting birds and summarizes some Diamond, J. M. 1975. Assembly of species
of the most compelling evidence on behalf communities. In Ecology and Evolution
of the importance of such species interac- of Communities, ed. M. L. Cody and J.
tions. M. Diamond, pp. 342–444. Cambridge,
Leisler, B., and H. Winkler. 1985. Ecomor- MA: Harvard University Press. This
phology. Current Ornithology 2:155–86. long chapter details many of the distribu-
To the extent that the Storer article below tional patterns for South Pacific birds. In
represents the past in studies of adaptive addition to presenting much interesting
avian morphology, this often complex arti- data on bird distributions and the appar-
cle presents the future in studies of adap- ent factors behind them, it has had some
tive avian morphology. Techniques for the management implications.
detailed study of the evolution of avian Diamond, J. M., and T. J. Case, eds. 1986.
form are presented, along with the sorts Community Ecology. New York: Harper
of correlations to be expected between dif- and Row. Although only portions of
ferent parts of the body. Ecomorphological this book deal with birds, it is the classic
patterns in different ecological situations discussion of the types of interactions that
are discussed, along with interactions can determine animal (and plant) distri-
between behavior and morphology. butions and lead to community structure.
Selander, R. K. 1971. Systematics and MacArthur, R. H., and E. O. Wilson. 1967.
speciation in birds. In Avian Biology, The Theory of Island Biogeography.
Suggested Reading

vol. 1, ed. D. S. Farner and J. R. King, Princeton, NJ: Princeton University

pp. 57–147. New York: Academic Press. Press. The theory of island biogeography
Although the first part of this chapter has had a tremendous impact on our
deals with material discussed in chapter understanding of distributional patterns
6, the second half is a fine review of the in birds, including recent work with man-
classical concepts of species and speciation agement. While this book does not deal
in birds. exclusively with birds, it is a landmark
publication in ecology.
432

1stPages_B.indd 432 7/22/20 11:59 AM

 Sanderson, J. G., and S. L. Pimm. 2015. Sibley, C. G., and J. E. Ahlquist. 1983.
Patterns in Nature: The Analysis of Spe- Phylogeny and classification of birds
cies Co-occurrences. Chicago: University based on the data of DNA-DNA hybrid-
of Chicago Press. A modern update to ization. In Current Ornithology, vol. 1,
the controversies discussed in some of the ed. R. F. Johnston, pp. 245–92. New
other selected readings for this chapter. York: Plenum. This article focuses on
the DNA-DNA hybridization technique.
The technique is described in detail, and
Chapter 6 its applications to avian systematics are
discussed. Several examples of taxonomic
Clements, J. F. 2007. The Clements Checklist changes suggested by DNA hybridization
of Birds of the World. Ithaca, NY: Cornell studies are presented.
University Press. This book presents
a list of all the birds of the world in one
Chapter 7
accepted taxonomic format, plus a limited
amount of information on the distribution
Brown, J. L. 1964. The evolution of diver-
of each species.
sity in avian territorial systems. Wilson
Corbin, K. W. 1983. Genetic structure and
Bulletin 76:160–69. This classic paper is
avian systematics. In Current Orni-
still an excellent introduction to the con-
thology, vol. 1, ed. R. F. Johnston, pp.
cept of cost-benefit analyses and territorial
211–44. New York: Plenum. This article
behavior.
is valuable primarily as a view to the past,
Krebs, J. R., and N. B. Davies. 1981. An
as it focuses on electrophoretic studies and
Introduction to Behavioural Ecology.
avian systematics. Electrophoretic tech-
Sunderland, MA: Sinauer Associates.
niques are reviewed and their applications
Although not directly dealing with birds,
in systematic studies are discussed.
this introductory text has excellent chap-
Hackett, S., R. T. Kimball, S. Reddy, R. C.
ters that deal with optimal foraging, the
Bowie, E. L. Braun, J. L. Chojnowski,
group-territory decision, and some of the
W. A. Cox, et al. 2008. A phylogenomic
problems associated with group dynamics.
study of birds reveals their evolutionary
Krebs, J. R., D. W. Stephens, and W. J.
history. Science 320:1763–68. This short
Sutherland. 1983. Perspectives in
paper presents some of the most recent
optimal foraging. In Perspectives in
discoveries on avian systematics using
Ornithology, ed. A. H. Brush and G. A.
massive amounts of molecular sequencing
Clark, pp. 165–216. Cambridge: Cam-
data.
bridge University Press. This review
Raikow, R. J. 1985. Problems in avian clas-
serves as a survey of the studies done
sification. In Current Ornithology, vol.
on various aspects of optimal foraging
2, ed. R. F. Johnston, pp. 187–212. New
through 1981. It is not a thorough review
York: Plenum. Although a bit dated,
of concepts but does serve as an excellent
as most of the material discussed here
introduction to the optimal foraging litera-
Suggested Reading

was before the development of molecular

ture.
techniques, this paper does an excellent
job in reviewing the major approaches to
systematic studies and their strengths and
Chapter 8
weaknesses. Discussion also covers the
many problems associated with making Lanner, R. M. 1996. Made for Each Other:
major changes in taxonomic classifica- A Symbiosis of Birds and Pines. Oxford:
tions that had been accepted for decades. Oxford University Press. A pleasant

433

1stPages_B.indd 433 7/22/20 11:59 AM

 review of the symbiosis between nutcrack- Moreau, R. E. 1972. The Palearctic-African
ers and jays and pines. Bird Migration Systems. New York:
Academic Press. This volume describes
Chapter 9 many of the patterns of migration in
birds breeding in Eurasia and wintering
Berthold, P. 1975. Migration: Control and in Africa. Emphasis is on the ecology
metabolic physiology. In Avian Biology, and distributional patterns of the species
vol. 5, ed. D. S. Farner, J. R. King, and that migrate in this region. Although this
K. C. Parkes, pp. 77–128. New York: volume does not offer the modern expla-
Academic Press. This chapter serves as nations of the Keast and Morton volume
an excellent introduction to some of the listed above, comparisons between the
physiological and behavioral aspects of African and American migration systems
migration. are often of interest.
Emlen, S. T. 1975. Migration: Orientation
and navigation. In Avian Biology, vol. Chapter 10
5, ed. D. S. Farner, J. R. King, and K.
C. Parkes, pp. 129–219. New York: Carey, C. 1980. Adaptation of the avian
Academic Press. This lengthy chapter egg to high altitude. American Zool-
serves as an excellent review of the many ogist 20:449–59. This paper is from a
aspects of orientation and navigation. symposium on the avian egg. The entire
Major sections discuss the navigational symposium is published as vol. 20 of the
capabilities of migrants and the cues they American Zoologist and contains many
use in finding direction. interesting papers on the structure and
Greenberg, R., and P. Marra, eds. Birds of function of the egg.
Two Worlds. 2005. Baltimore: Johns Epple, A., and M. H. Stetson, eds. 1980.
Hopkins University Press. The most Avian Endocrinology. New York: Aca-
recent of several symposium volumes on demic Press. This book and the one
migrant birds that have appeared since listed below are collections of papers from
Keast and Morton, this one includes much scientific symposia and provide a wealth of
concern about migrant bird conservation information on male and female repro-
in addition to modern advances in under- ductive physiology, photoperiodic control
standing the details of bird migration. of reproductive cycles, and so forth.
Keast, A., and E. S. Morton, eds. 1980. Nikami, S. K., K. Homna, and M. Wade,
Migrant Birds in the Neotropics: Ecology, eds. 1983. Avian Endocrinology: Envi-
Behavior, Distribution and Conservation. ronmental and Ecological Perspectives.
Washington, DC: Smithsonian Institu- Tokyo: Japan Scientific Press.
tion Press. This volume of 40 papers from O’Connor, R. J. 1984. The Growth and Devel-
a 1978 symposium totally changed how opment of Birds. New York: Wiley. This
ornithologists understood migrant birds. excellent text covers all aspects of prenatal
Among the many topics considered are and postnatal development in birds.
Suggested Reading

migratory patterns of different taxonomic Phillips, J. C., P. J. Butler, and P. J. Sharp.

groups, patterns of migration in different 1985. Physiological Strategies in Avian
regions, the implications of wintering in Biology. Glasgow, Scotland: Blackie and
the tropics, and models for the evolution Sons. The two chapters on reproduction
of these migratory systems. While many in this text discuss the endocrine regula-
questions about migratory behavior are tion of avian reproduction and the influ-
answered, many more are posed. ence of environment on breeding cycles.

434

1stPages_B.indd 434 7/22/20 11:59 AM

 Chapter 11 in an attempt to see how general they are
in occurrence and how well they can be
Armstrong, E. A. 1965. Bird Display and explained by current hypotheses.
Behavior. New York: Dover. Although Cody, M. L. 1966. A general theory of
much of this book is conceptually out of clutch size. Evolution 20:174–84. In
date, it still provides excellent descriptions addition to presenting the model discussed
of many of the basic displays and other in the text, this paper has an excellent
behavior that accompany avian reproduc- review of the various explanations offered
tion. for latitudinal variation in clutch size
Kroodsma, D. 2005. The Singing Life of prior to 1966.
Birds. Boston: Houghton Mifflin. Sub- Emlen, S. T., and S. L. Vehrencamp. 1983.
titled “The Art and Science of Listening to Cooperative breeding strategies among
Bird Song,” this is a very entertaining look birds. In Perspectives in Ornithology,
at one man’s studies of bird song across ed. A. H. Brush and G. Clark Jr., pp.
North America, with lots of good science 93–133. Cambridge: Cambridge Uni-
within some good personal stories. versity Press. A great number of papers
Kroodsma, D. E., and E. H. Miller, eds. reviewing the occurrence of cooperative
1982. Acoustic Communication in Birds. breeding appeared in the 1980s. This
Vols. 1 and 2. New York: Academic article does as good a job as any of present-
Press. This two-volume sets covers all ing some examples and pointing out the
aspects of avian communication in detail. relevant questions involved in studies of
Vol. 1 focuses on production, perception, cooperative breeders.
and design features of sounds, with nine Lack, D. 1968. Ecological Adaptations for
chapters on these topics. Vol. 2 deals with Breeding in Birds. London: Methuen.
song learning and its consequences, with This book presents an excellent introduc-
nine chapters and an appendix. Although tion to many of the breeding adaptations
these chapters are occasionally detailed, we have discussed in this chapter. As
much of the material is written at a level many of the theoretical advances in this
that most biologists can understand. area occurred after 1968, it is somewhat
Slater, P. J. B. 1983. Bird song learning: out of date in concept, but it still provides
Theme and variations. In Perspectives in many excellent examples of adaptations.
Ornithology, ed. A. H. Brush and G. A. Ligon, David. 1999. The Evolution of Avian
Clark, pp. 475–511. Cambridge: Cam- Breeding Systems. Oxford: Oxford Uni-
bridge University Press. This article is versity Press. A broad review of all the
an excellent introductory review of the avian breeding systems and how and why
current state of knowledge on bird song they occur.
learning. It is followed by commentary by Oring, L. W. 1982. Avian mating systems.
Luis Baptista and Donald Kroodsma. In Avian Biology, vol. 6, ed. D. S.
Farner, J. R. King, and K. C. Parkes, pp.
Chapter 12 1–92. New York: Academic Press. This
Suggested Reading

article provides a lengthy review of both

Clark, A. B., and D. S. Wilson. 1981. the occurrence of various mating systems
Avian breeding adaptations: Hatching in birds and the ecological and evolution-
asynchrony, brood reduction, and nest ary pressures at work in determining these
failure. Quarterly Review of Biology systems.
56:253–77. This article reviews the mate- Ortega, C. P., J. F. Chace, and B. D. Peer.
rial on various brood reduction strategies 2005. Management of Cowbirds and

435

1stPages_B.indd 435 7/22/20 11:59 AM

 Their Hosts: Balancing Science, Ethics, of the factors limiting such traits.
and Mandates. Ornithological Mono- Perrins, C. M., and T. R. Birkhead. 1983.
graphs 57. Washington, DC: American Avian Ecology. Glasgow, Scotland:
Ornithologists’ Union. A recent evalua- Blackie and Sons. This introductory text
tion of the damage done by cowbirds and has sections covering nearly all the topics
how managers deal with this brood para- discussed in this chapter.
site when it is the main cause of a species’ Winkler, D. W., and J. R. Walters. 1983. The
decline toward endangered status. determination of clutch size in preco-
Parker, P. G., and N. T. Burley. 1998. Avian cial birds. In Current Ornithology, vol.
Reproductive Tactics: Female and Male 1, ed. R. F. Johnston, pp. 33–68. New
Perspectives. Ornithological Mono- York: Plenum. This article reviews recent
graphs 49. Washington, DC: American theories on clutch size, with an emphasis
Ornithologists’ Union. A set of papers on on theories dealing with clutch size in
various tactics used by monogamous birds. precocial birds.
Payne, R. B. 1984. Sexual Selection, Lek and
Arena Behavior, and Sexual Size Dimor- Chapter 13
phism in Birds. Ornithological Mono-
graphs 33. Washington, DC: American Cocker, M. 2013. Birds and People. London:
Ornithologists’ Union. Several of the Jonathan Cape.
topics associated with sexual selection in Lebbin, D. J., M. J. Parr, and G. H. Fenwick.
birds are addressed in this monograph, 2010. The American Bird Conservancy
with information on both the adaptive Guide to Bird Conservation. Chicago:
value of sexually selected traits and some ­University of Chicago Press.
Suggested Reading

436

1stPages_B.indd 436 7/22/20 11:59 AM

 INDEX

Note: Page numbers in italics indicate Allen’s rule, 218

illustrations. allopatric populations: continental drift
and, 111, 112, 114; defined, 86; ecological
acceleration phase of reproduction, 306, factors in promotion of, 90, 111; genetic
307 patterns in, 168; on islands, 107; Pleis-
Acorn Woodpecker (Melanerpes formiciv- tocene glaciation and, 101–3, 102; in
orus), 234, 235, 238, 377, 380 tropical America, 106
acoustic environment, 317–18, 324 allopatric speciation, 101, 105, 108
ACTH (adrenocorticotropic hormone), 57, alpha diversity, 144–46
58 alternate plumage, 25
adaptations, 216–38; behavioral, 220–22, altitudinal gradients, 152–53, 324
228–29, 234, 324–25, 340; to cold, altricial birds: brood parasitism and, 383;
217–27; for flight, 19–20, 44, 78, characteristics upon hatching, 298,
258; to food shortages, 216–17; for 299; clutch size and, 358; digestive sys-
food storage, 234–38; to heat, 227–31; tem in, 302; egg size and structure of,
to human-modified habitats, 399; 292, 299; embryonic development of,
morphological, 78, 218–20, 228, 231, 296, 299; incubation of, 338; nestling
387; physiological, 222–33, 258; from period in, 299–301, 339, 342; prolactin
radiation, 114–25; tool use for foraging, levels and, 308
215; to xeric conditions, 231–34. See also altruism, reciprocal, 199
evolution alula, 67, 70, 72, 80
Adelie Penguin (Pygoscelis adeliae), 193 American Birding Association, 177, 398
adrenal gland, 58 American Crow (Corvus brachyrhynchos),
adrenocorticotropic hormone (ACTH), 57, 85–86
58 American Dipper (Cinclus mexicanus), 55
aerial maneuvers, 71 American Goldfinch (Carduelis tristis),
aeroelastic flutter, 23 222–23, 360
African Gray Parrot (Psittacus erithacus), American Ornithological Society (AOS), 10,
48, 51 86, 88, 177, 399
African Penduline-tit (Anthoscopus caroli), American Redstart (Setophaga ruticilla), 26,
336 172, 243, 256, 276
afterfeathers (aftershafts), 20–22, 21 American Robin (Turdus migratorius), 34,
aggregations, 206 347, 360
aggressive neglect, 198 anatomy and physiology, 19–59; adapta-
Ahlquist, Jon, 164, 167 tions for flight, 19–20; circulatory
alarm calls, 199 system, 41–43; digestive system, 19,
albatrosses: brood patch of, 289; courtship 33–37, 302; of egg production, 279–84;
behavior of, 333; dynamic soaring endocrine glands, 47, 56–59, 284; feet,
by, 75; hatching process for, 297; salt 11, 20, 23, 71, 115–16, 228; legs, 23,
glands in, 232; smell ability in, 51; take- 46, 70, 115, 116; muscular system, 19,
offs by, 71; timing of breeding by, 361 44–47; nervous system, 47–50; repro-
albumen, 281, 290–91, 294 ductive systems, 280–83; respiratory

437

1stPages_B.indd 437 7/22/20 11:59 AM

 system, 38–40, 42; shape and form, Barn Owl (Tyto alba), 23, 56, 57, 395
29, 30; skeletal system, 19, 30–33, 32; Bar-tailed Godwit (Limosa lapponica), 247
skin, 22–23, 27–29, 50; tail, 46, 71, 123; basic plumage, 25
urinary system, 43–44. See also bills; beaks. See bills
feathers; sensory organs; wings Bee Hummingbird (Mellisuga helenae), 63
Andean Hillstar (Oreotrochilus estella), 220 behavioral adaptations: to cold, 220–22;
androgens, 58, 282, 306 dialect and, 324–25; to heat, 228–29;
angle of attack, 66, 67, 70, 71 imprinting, 340; to xeric conditions,
anis, 222, 376, 380 234
anisodactyl feet, 115, 116 behavioral ecology, 264–65
Anna’s Hummingbird (Calypte anna), 243, Bell Miner (Manorina melanophrys), 198
245, 332 Bergmann’s rule, 218
antihunting arguments, 396–97 beta diversity, 145
antiperistalsis, 35–36, 233 bet-hedging strategies, 198, 358–59
antwrens, 94 Bewick’s Swan (Cygnus columbianus), 306
AOS. See American Ornithological Society bicoordinate navigation, 266, 268
Aquatic Warbler (Acrocephalus paludicola), bills: adaptations in, 95, 116–23; coloring
284 on, 28; digestive system and, 33–34;
arboreal theory of flight, 12, 65 food habits and, 95, 116–23, 246; size
Archaeopteryx, 3, 6–10, 12–13, 16, 20, 112 and shape variations, 28, 110, 396;
Archaeornithura meemannae, 16, 17 touch receptors on, 50
archosaurs, 5, 7, 9, 12 binocular vision, 53, 54
Arctic Tern (Sterna arctica), 247 biogeographical studies, 131–33, 403–4
arginine vasotocin, 57, 307 biological species concept (BSC), 85–86,
arrival-time hypothesis, 253, 256 157, 163, 176–77
artificial nests, 405 bipedalism, 1, 5, 9, 13, 65
artificial selection, 391–93 birds: conservation efforts, 275–78, 277,
assembly rules of guild structure, 133–34, 397, 405, 408; domestication of, 306,
139 390–94; ecosystem roles of, 394–95;
Association of Field Ornithologists, 399 energy metabolism in, 59–64, 216;
assortative mating, 324, 325 extinction events impacting, 18; for
Atlantic Puffin (Fratercula arctica), 120, 406 food purposes, 390–93; habitat require-
attendant species, 206 ments, 400–404, 401; hunting for
auditory ability. See ears game birds, 396–97; intelligence of,
auditory template, 326, 327 47–48; management practices, 275–76,
auks, 80, 180–81 399–400, 402–6; origins of, 2–8; as
Australian Superb Lyrebird (Menura novae- pets, 392–94; reptilian ancestry of,
hollandiae), 328 3–6. See also anatomy and physiology;
avian. See birds evolution; flight; foraging behavior;
migration; reproduction; speciation;
Bald Eagle (Haliaeetus leucocephalus), 26, taxonomy; specific species and types of
60 birds
Bananaquit (Coereba flaveola), 34, 109, 118 birds of prey, 29, 54, 182, 280, 332, 350
Bank Swallow (Riparia riparia), 289 birdsong, 316–29; dialects, 87, 319, 322,
barbicels, 20, 22 324–25; duetting, 327–28; functions of,
barbs, 20, 22, 50 316–17, 321, 322; learning, 325–27; in
Index

barbules, 20, 22 mating behavior, 162, 316–17, 324–25;

Barheaded Goose (Anser indicus), 40 mimicry, 328–29; natural selection

438

1stPages_B.indd 438 7/22/20 11:59 AM

 and, 317, 321, 322; territorial behavior body-size hypothesis, 253, 255, 256
and, 316, 320; variation in, 317–25, 323. bones. See skeletal system
See also songbirds boobies, 181, 230, 331, 333
bird-watching, 145, 261, 398 bowerbirds, 370, 371
bitterns, 54 brain structures, 47–50
Black-and-white Warbler (Mniotilta varia), breathing. See respiratory system
172, 243, 276 breeding: aeroelastic flutter and, 23; arrival
Black-billed Magpie (Pica pica), 62 at breeding grounds, 193; captive
blackbirds: aggressive neglect among, 198; breeding, 405; domesticated species,
brood parasitism and, 384; fledgling 391, 392; foraging behavior and, 187,
period in, 303; in mating studies, 365; 189–90; group systems of, 194, 375–83;
migration of, 239; natural selection helpers in, 194, 375, 376, 378–82;
among, 84; scientific names, 86; inbreeding, 325; plumage during, 25,
systematic studies of, 162; territorial 204; territorial behavior during, 195,
behavior of, 191, 197 311–12, 316, 377–83; timing of, 360–62.
Black-capped Chickadee (Poecile atricap- See also nesting colonies; reproduction
illus): coexistence with other species, bristles, 21, 22, 50, 120
95; in cold climates, 224, 227; energy brooding behavior, 5, 57, 301, 339, 341, 388
demands of, 63; extra-pair young brood parasitism, 383–88
among, 364; foraging behavior of, 217; brood patch, 50, 57, 289, 308
habitat requirements, 400; zone of brood reduction mechanisms, 358–59
contact among, 103, 104 Brown, Jerram, 188–89, 311
Black-capped Vireo (Vireo atricapilla), 384 Brown-headed Cowbird (Molothrus ater),
Black-headed Duck (Heteronetta atricapilla), 384, 385
384 Brown Pelican (Pelecanus occidentalis), 230,
Blackpoll Warbler (Setophaga striata), 240, 343
241, 258, 259, 262, 264 Brown Thrasher (Toxostoma rufum), 328
Black Swan (Cygnus atratus), 306 BSC. See biological species concept
Black-throated Blue Warbler (Setophaga Budgerigar (Melopsittacus undulatus), 43,
caerulea), 151 234
Black-throated Sparrow (Amphispiza bilin- Bunning, Erwin, 304
eata), 234 buntings, 26, 105, 168, 169, 244, 268
blood components, 41–42 bustards, 34, 173, 179
blood pressure, 19, 41, 49, 58
Blue-and-white Flycatcher (Cyanoptila Cackling Goose (Branta hutchinsii), 88, 90
cyanomelana), 151 calamus, 20, 22
bluebirds, 214, 220, 221 California Condor (Gymnogyps califor-
Blue-black Grassquit (Volatinia jacarina), nianus), 405
109 camber, 66–67, 74–76
Blue Bunting (Cyanocompsa cyanoides), Canada Goose (Branta canadensis), 88, 90,
168, 169 156
Blue-footed Booby (Sula nebouxii), 331, 333 canaries, 321, 327, 393
Blue Grosbeak (Guiraca caerulea), 360 Canvasback (Aythya valisineria), 243
Blue-headed Quail Dove (Starnoenas cyano- caprimulgids, 224, 226, 230
cephala), 47 captive breeding, 405
Blue Jay (Cyanocitta cristata), 218 caracaras, 183
Index

Blue Tit (Parus caeruleus), 302–3, 312 Carolina Chickadee (Poecile carolinensis),
Bock, Walter, 15 95, 103, 104, 218

439

1stPages_B.indd 439 7/22/20 11:59 AM

 Carrion Crow (Corvus corone), 56 interspecies diversity in, 353–55; intra-
cassowaries, 80, 178 specific variation in, 355–58; migration
cavity nesters: artificial nests for, 405; and, 272; natural selection and, 345;
clutch size of, 355; in cold climates, optimal, 351–52; reproductive success
220–22; egg shape of, 293; growth rate as function of, 271; seasonal variation
for, 301; in hot conditions, 229; site in, 285; tactile influences on, 50. See
dominance among, 271 also eggs
cecum, 35–37 CNS (central nervous system), 48
central nervous system (CNS), 48 cochlea, 55, 56
central place foraging (CPF), 211–12 Cody, Martin, 357
cerebellum, 49 coelurosaurs, 9–11, 10
Chaffinch (Fringilla coelebs), 325–26 coevolution, 117, 147–48, 265
character displacement, 97–100, 139 cold, adaptations to, 217–27
checkerboard patterns of distribution, 134, colies, 182
135, 139 colonial nesting. See nesting colonies
Chestnut-eared Finch (Taeniopygia castano- Common Bushtit (Psaltriparus minimus),
tis), 231 221
chickadees: coexistence with other species, Common Eider (Somateria mollissima), 336
95; in cold climates, 218, 224, 227; Common Grackle (Quiscalus quiscula), 359
energy demands of, 63; extra-pair Common Murre (Uria aalge), 293, 294
young among, 364; feather weight to Common Nighthawk (Chordeiles minor),
body mass ratio, 218–19; feeding of 122, 329
nestlings by, 341; food storage by, 238; Common Poorwill (Phalaenoptilus nuttallii),
habitat requirements, 400; in optimal 226, 231
foraging studies, 209; tool use among, Common Redpoll (Carduelis flammea), 220
215; zone of contact among, 103, 104 Common Swift (Apus apus), 37
chickens: blood pressure in, 41; dominance communal roosting, 220–22
hierarchies among, 204; economic community ecology, 126, 130, 144, 154
value of, 393; egg production in, 281, competition: in Andean bird community,
282, 291, 307; feather structure, 22; 152–53; birdsong and, 320; in group
muscular system of, 45; precocial, breeding systems, 380; intrabrood, 359;
298–99; prevalence of, 392–93; repro- intraspecific, 274; patterns of, 136, 142;
ductive organs of, 280; size of, 392; in polygyny, 370, 371; speciation and,
skeletal system of, 32; taste buds in, 91–93, 97–100, 127; territorial behavior
51; taxonomic classification, 178; urine and, 189, 191
composition in, 44 competitive exclusion principle, 91–93,
circulatory system, 41–43 152–53
cladistics, 160–61 condors: captive breeding of, 405; ecosys-
Clark’s Nutcracker (Nucifraga columbiana), tem role of, 395; egg laying by, 284;
23, 235–37, 360 energy demands of, 64; soaring ability
classification. See taxonomy of, 76, 79; timing of breeding by, 361
The Clements Checklist of Birds of the World, connectivity, in migration studies, 276–78,
177–86 277
climate change, 265, 399 conservation efforts, 275–78, 277, 397, 405,
clock-shift experiments, 267 408
clutch size, 351–59; bet-hedging strategies continental drift, 90, 111–14, 399
Index

and, 358–59; fledgling weight and, 352, contour feathers, 21, 22, 24, 29
353; geographic influences on, 355–58; convergence: in birdsong, 318, 328–29; eco-

440

1stPages_B.indd 440 7/22/20 11:59 AM

 logical, 149; morphological, 149, 158; in dialects, 87, 319, 322, 324–25
signaling, 197; at species level, 82, 149, Diamond, Jared, 97, 133, 136, 141, 371
151–52; of territorial boundaries, 206; Diatryma, 81, 82
trophic, 145 diet. See food
cooperative breeding systems, 194, 375–83 digestive system, 19, 33–37, 302
coots, 179 digits, evolution of, 11
copulation: anatomy and physiology of, dinosaurs, 2–13, 4, 15–18, 20, 81
283–84; courtship behavior and, 330, directional selection, 84
333; extra-pair, 363, 364; fertilization discriminators, 384–85
period following, 284; in leks, 369; dispersal movements, 240
locations for, 333–34; in nesting colo- displacement patterns, 92–93, 127
nies, 315; territorial behavior and, 312. distraction displays, 336, 337, 339
See also mating behavior diversity: alpha, 144–46; altitudinal gra-
cormorants, 80, 120, 181, 230 dients in, 152–53, 324; beta, 145; of
Cornell Lab of Ornithology, 177, 276, 398 birdsong, 317–25, 323; constraints on,
corpus striatum, 48–49 126–30, 140, 144; of courtship behav-
cost of intrusion, 194 ior, 330–33, 331; defined, 126; gamma,
cotylosaurs, 3–4 144–46; of habitats, 110; latitudinal
courtship behavior: functions of, 330, gradients in, 145–49, 150, 356–57; mea-
333–34; genetic influences on, 162; sures of, 126; from radiation, 114–25;
hormonal influences on, 306; nonvocal single-location studies of, 153–54;
sounds in, 329; in reproductive cycle, speciation rates in determination of,
304; secondary sex characteristics in, 126–27. See also speciation
282, 333; variation of, 330–33, 331. See diving birds, 52, 70–71, 173
also mating behavior DNA: hybridization, 164–66, 167, 175;
cowbirds, 275, 384–86 molecular structure of, 163, 164;
Cox, George, 107 sequencing, 87, 173–75, 176
CPF (central place foraging), 211–12 Dodo (Raphus cucullatus), 123
cranes, 39, 173, 179, 289, 332 domesticated birds, 306, 390–94
creepers, 218, 220–21 dominance. See site dominance
Cretaceous-Tertiary (K-T) boundary, 18 dominance hypothesis, 255, 256
crop, 35, 36 Double-banded Courser (Rhinoptilus afri-
crossbills, 107, 122–23, 124, 240, 246 canus), 287
crows: eyes of, 54; hearing ability of, 56; doves: exotic species of, 394; gular flut-
intelligence of, 48; migration of, 257; ter utilized by, 230; hunting of, 396;
navigation and orientation among, incubation of eggs, 287, 288; prolactin
265–66; scientific names, 85–86; tool levels in, 308; reproduction in, 309;
use among, 215 taxonomic classification, 173, 179;
cuckoo-rollers, 182 timing of breeding by, 360; wing shape
cuckoos, 173, 179, 344, 384–87 of, 74
cursorial theory of flight, 12–13, 20, 65 down feathers, 21, 22, 339
Czerkas, Stephen, 15 Downy Woodpecker (Picoides pubescens),
218
Dark-eyed Junco (Junco hyemalis), 255 ducks: bills of, 50, 123; brood parasitism
Darwin, Charles, 9, 108, 110, 140, 156, 175 and, 384, 387; domesticated, 390;
delayed maturation, 203, 371, 377 feather structure, 22; flightless, 80;
Index

determinate layers, 285, 336 hunting of, 396; mating behavior

Dial, Ken, 13 of, 329; molting process of, 24, 25;

441

1stPages_B.indd 441 7/22/20 11:59 AM

 monogamy among, 367–68; philopatry einschlaufpause, 263
among, 243; precocial, 298–99; repro- electrophoretic techniques, 163–65
duction in, 282, 284, 345; taxonomic Eleonora’s Falcon (Falco eleonorae), 360
classification, 178; tongue of, 33–34; Elephant Bird (Aepyornis maximus), 81, 82,
urine composition in, 44 292
duetting, 327–28 elliptical wings, 72–74, 73, 78
Dunnock (Prunella modularis), 382–83 embryonic development, 285, 286, 294–97
duodenum, 35, 36, 59 Emlen, Stephen, 362
dynamic soaring, 75, 77, 79, 264 Emperor Penguin (Aptenodytes forsteri), 36,
63–64, 222
eagles, 26, 60, 119, 284 emus, 80
ears, 55–56, 57, 159 enantiornithines, 16–18, 17
Eastern Bluebird (Sialia sialis), 214, 221 endangered species, 400, 406–8
Eastern Meadowlark (Sturnella magna), endocrine glands, 47, 56–59, 284. See also
103, 218 hormones
Eastern Phoebe (Sayornis phoebe), 334, 364 energy metabolism, 59–64, 216
eating habits. See food environmental potential for polygamy
echolocation, 56 (EPP), 362–66, 370, 373, 375, 388
eclipse plumage, 25 EPCs (extra-pair copulations), 363, 364
ecological constraints, 130, 144 EPY (extra-pair young), 363, 364
ecological convergence, 149 equilibrium (physiological), 55
ecological isolation, 92–97, 100–103, equilibrium model, 131–33, 403
126–28, 138 esophagus, 34–36, 37
ecological niches, 91–93, 108, 127 estrogens, 58, 59, 289, 306, 308
ecology: behavioral, 264–65; community, European Kestrel (Falco tinnunculus), 54
126, 130, 144, 154; geographical, 144; European Starling (Sturnus vulgaris), 212,
landscape, 402–4 265–66, 347
ecomorphology, 114, 125 evolution: coevolution, 117, 147–48, 265;
ecosystem roles, 394–95 of feathers, 9, 11–12, 20; of flight,
eggs, 279–99; anatomy and physiology of 12–13, 20, 65; of helping behavior, 379;
production, 279–84; brood parasitism of migration, 249, 259, 270–75, 273;
and, 383–88; color variations among, neoteny process and, 81–82; of polyg-
293–94, 336; in domesticated species, yny, 191, 365–70; radiation patterns
392; economic value of, 390, 393; and, 16–18, 111–14; of systematics and
embryonic development, 285, 286, taxonomy, 156–57; of territorial behav-
294–97; hatching, 296–99; laying of, ior, 188, 189–90, 312; theories of bird
50, 284–85, 336–38; sensory contact evolution, 8–16, 14; of wings, 1, 12–13.
with brood patch, 50; size and shape See also adaptations; natural selection
of, 291–93; structure of, 290–91, 292; excretion, 43–44, 232–33
texture of, 291, 293; yolk of, 280–82, external coincidence model, 305
290–91, 295, 296, 299. See also clutch extinction: agents of, 399, 406–8; attributes
size; incubation; nest building of extinct species, 406–7; ecological
eggshell, 33, 59, 281, 282, 291, 292 interactions and, 127; in equilibrium
egg tooth, 2, 297 model, 131–32; of flightless birds,
Egyptian Plover (Pluvianus aegyptius), 287, 80–81; K-T boundary and, 17–18
338 extra-pair copulations (EPCs), 363, 364
Index

Egyptian Vulture (Neophron percnopterus), extra-pair young (EPY), 363, 364

215 eyes, 26–27, 51–55, 53

442

1stPages_B.indd 442 7/22/20 11:59 AM

 falcons, 173, 183, 199, 360 264; takeoffs, 45, 67, 70–71; undulat-
fallouts, 261 ing, 78; variations in technique, 71–79.
feathers: in breeding displays, 23; clean- See also wings
ing, 28; color of, 25, 26–27; as distinct flight feathers, 20, 29, 50, 69–70, 309, 344
avian trait, 1, 11; economic value of, flightless birds, 15, 79–82
393; evolution of, 9, 11–12, 20; flight, floaters, 193–96, 377
20, 29, 50, 69–70, 309, 344; insulative flock foraging: breakdown of territorial
value of, 20, 219–20; molting process, behavior and, 191; dominance hierar-
24–26, 243, 309; as percentage of body chies in, 204–5; factors affecting flock
weight, 218–19; structure of, 20–22, 21, size, 201–2; mixed-species, 205–6, 207;
23; waterproofing, 28. See also plumage for predator defense, 188, 198–201,
Feduccia, Alan, 10, 13, 15 200, 311; resource distribution and,
feet, 11, 20, 23, 71, 115–16, 228 188, 190, 198, 311; status signaling and,
female defense polygyny, 369 204–5
female reproductive system, 280–82 Florida Scrub-Jay (Aphelocoma coerulescens),
fertilization, 281–84, 294, 330, 363, 368 47, 194, 378, 379
filoplumes, 21, 22, 50 flowerpeckers, 36, 117, 118
finches: bills of, 124; brood parasitism and, flufftails, 179
384, 386, 387; in cold climates, 218–20; follicle-stimulating hormone (FSH), 57,
community patterns among, 140; cool- 281, 306
ing strategies of, 231; distribution of, food: bill design and, 95, 116–23, 246;
92, 100; foraging behavior of, 215, 246; clutch size and, 353–54; courtship feed-
heat production capabilities, 222–23; ing, 332–34; digestive system and, 19,
migration of, 253, 304; molecular 33–37; ecological isolation by, 94–96;
studies of, 175, 176; oral cavity among, energy needs and, 62–64; growth rates
34; in pet trade, 394; in photoperiod in relation to, 301, 302; migration in
studies, 305; radiation among, 108–10; relation to, 245–47, 260, 271–72; for
reproduction in, 304, 350; song learn- nestlings, 234, 311, 339–42, 343; optimal
ing by, 325–26 choice of, 209–11; preformed water in,
fitness. See reproductive success 231; shortages, 216–17; site dominance
Fitzpatrick, John, 378 and, 271–72; size and quantity avail-
flamingos: bills of, 121, 123; black wing tips able, 125, 140, 141; storage adaptations,
among, 25; color of, 26; esophagus 234–38; territoriality and distribution
among, 36; taxonomic classification, of, 188–91, 311; timing of breeding in
173, 179; tongue of, 33–34 relation to, 360–61; use of birds for,
fledglings: in breeding groups, 379; brood 390–93. See also foraging behavior
parasitism and, 386–87; clutch size foraging behavior, 187–215; bill design and,
and weight of, 352, 353; parental care 116–23; ecological isolation by, 93–97,
of, 275–76, 303, 344; sensitive periods 98; efficiency of, 187, 198, 199; general
for, 326 patterns, 188–91; guilds and, 136, 137,
flickers, 102–3, 105 145, 153; hyperphagia and, 264; location
flight, 65–79; adaptations for, 19–20, 44, decisions, 211–13; of migrants, 264–65;
78, 258; aerial maneuvers, 71; ener- in nesting colonies, 198, 315; optimal
gy-saving behavior, 78–79; evolution of, models of, 187, 188, 207–15; status sig-
12–13, 20, 65; gliding, 65–68; hovering, naling and, 202–5; territorial, 188–98,
40, 45, 78; landings, 67, 71; muscles 202–3, 311; tool use strategies, 215. See
Index

for, 19, 44–45, 46; powered, 68–70; res- also flock foraging; food
piration during, 42; soaring, 45, 75–79, formation flying, 78

443

1stPages_B.indd 443 7/22/20 11:59 AM

 fovea, 52, 54 Greater Roadrunner (Geococcyx califor-
Fraser Darling effect, 315 nianus), 222
Fretwell, Steve, 239 Greater Vasa Parrot (Coracopsis vasa), 284
frigatebirds: courtship behavior of, 331; Great Horned Owl (Bubo virginianus), 217,
landings by, 71; nesting colonies of, 313; 288, 360
taxonomic classification, 181; timing of Great Tit (Parus major): clutch size of, 285,
breeding by, 361–62; wing loading of, 352, 353; feeding of nestlings by, 341;
77–78 foraging behavior of, 209, 211, 212;
FSH. See follicle-stimulating hormone incubation of eggs, 338, 339; territorial
furcula, 7, 30, 35 behavior of, 196, 316, 320
grebes: brood patch of, 289; courtship
Galapagos Hawk (Buteo galapagoensis), 193, behavior of, 330–32, 331; flightless, 80;
381–82 precocial, 298–99; takeoffs by, 70–71;
Galapagos Swallow-tailed Gull (Creagrus taxonomic classification, 173, 179
furcatus), 56 Green Jay (Cyanocorax yncas), 215, 380
galliforms, 230, 284, 289 Green Woodhoopoe (Phoeniculus purpu-
gallinules, 179 reus), 376, 377
game birds, 13, 173, 396–97 Greylag Goose (Anser anser), 390
gamma diversity, 144–46 grosbeaks, 34, 124, 240, 360
Gause, G. F., 91 group breeding systems, 194, 375–83
geese: domesticated, 390, 393; egg pro- group foraging. See flock foraging
duction in, 282, 284; flightless, 80; grouse: in cold climates, 220; feeding of
flying altitude of, 264; formation flying nestlings by, 342; imprinting among,
by, 78; hunting of, 396; imprinting 340; intestinal tract of, 37; pellet forma-
among, 340; migration of, 40, 239, tion and regurgitation in, 36; polygyny
258, 260; monogamy among, 367; pair- among, 371
bonds among, 329; subspeciation, 88, growth rates, 299–303, 315, 342
90; taxonomic classification, 156, 178 guilds, 133–40, 142, 143, 145, 153
genetic monogamy, 363, 364, 376 gular flutter, 229–31, 287
genetic polygyny, 363, 364 gulls: breeding systems among, 382; brood
genomics, 172–75 patch of, 289; cooling strategies of,
genotypes, 83, 84 228–29; echolocation among, 56; feed-
geographical ecology, 144 ing of nestlings by, 340; heart rate of,
geolocator studies, 278, 405 42; incubation of eggs, 285, 286; nest-
geomagnetic cues, 268–69 ing colonies of, 314; pellet formation
Giant Petrel (Macronectes giganteus), 227 and regurgitation in, 36; salt glands
gizzard, 20, 35–37, 122 in, 232; semiprecocial, 299; taxonomic
glandular stomach, 35, 37, 59 classification, 180–81
gliding, 65–68
global warming, 265 habitats: birdsong frequencies and, 318;
glucagon, 35, 59 diversity of, 110; ecological isolation
goatsuckers, 36, 179 by, 93–94; geographic distribution of,
goldfinches, 124, 222–23, 227, 360 248–49, 250; human-modified, 399;
gonadotropin-releasing hormone (GnRH), migration effects and, 248–49; nest
306, 307 building influenced by, 334–35; optimal
Gray Jay (Perisoreus canadensis), 234 foraging locations, 211–13; population
Index

Great Auk (Pinguinus impennis), 80 fluctuations and, 347; requirements for,

Greater Flamingo (Phoenicopterus ruber), 36 400–404, 401; saturation of, 128; sepa-

444

1stPages_B.indd 444 7/22/20 11:59 AM

 ration of, 94, 97, 147. See also territorial Hooded Crow (Corvus cornix), 257, 265–66
behavior hoopoes, 159, 182
Haffer, Jürgen, 107 hormones: adrenal, 58; in brood patch
Hairy Woodpecker (Picoides villosus), 218 development, 289; pancreatic, 35, 59;
hamuli, 20, 22 parathyroid, 59; pituitary, 56–58, 281,
Harris’s Hawk (Parabuteo unicinctus), 68, 289, 307; in reproduction, 281, 306–8;
360, 381 in seasonal adaptations, 227; thyroid,
Harris’s Sparrow (Zonotrichia querula), 58. See also specific hormones
204–5 hornbills, 182, 388–89
hatching, 296–99 House Finch (Carpodacus mexicanus), 305
Hawaiian honeycreepers, 108, 110–11, 158, House Sparrow (Passer domesticus): in cold
160 climates, 220; dominance interac-
hawks: bills of, 119, 122; breeding behav- tions among, 205; egg production in,
ior of, 360, 381; brood patch of, 289; 281–82; energy expenditures by, 62, 63;
courtship behavior of, 332; eyes of, 53; flying altitude of, 40; heart size of, 42;
feeding of nestlings by, 342; flightless, reproductive organs of, 283; scientific
81; group breeding among, 381–82; naming of, 86; timing of breeding by,
intestinal tract of, 37; landings by, 68; 361
migration of, 247, 249, 258; pellet House Wren (Troglodytes aedon), 286, 329,
formation and regurgitation in, 36; 345, 355
semialtricial, 299; static soaring by, 76; hovering, 40, 45, 78
territorial behavior of, 193, 195; timing hummingbirds: aeroelastic flutter by, 23;
of breeding by, 360 bill size and shape of, 396; courtship
head muscles, 46 behavior of, 332; energy demands of,
hearing. See ears 62, 63; feather count, 29; as flower
heart and heart rate, 1, 19, 41–43 feeders, 117, 125, 213, 265; hovering by,
heat, adaptations to, 227–31 78; incubation of eggs, 288; intestinal
heat exchange, 227, 231, 289 tract of, 37; migration of, 243, 245, 253,
Heermann’s Gull (Larus heermanni), 258–59, 264, 274; nest building by,
228–29, 285 334, 335; polygyny among, 370; roosting
helpers, 194, 375, 376, 378–82 sites for, 220; size of, 78–79, 125; terri-
herons: in cold climates, 227; egg laying by, torial behavior of, 194; torpor utilized
284; eyes of, 54; gular flutter utilized by, 63, 79, 217, 224–25; wing shape of,
by, 230; nesting colonies of, 314; semi- 76, 77
altricial, 299; taxonomic classification, hunting for game birds, 396–97
181 Hutchinsonian ratios, 95, 138
Herring Gull (Larus argentatus), 42, 228, Huxley, Thomas, 9
286, 287 hyperphagia, 264
heterodactyl feet, 115, 116 hypersexuality, 392
hibernation, 226 hypothalamus, 57–58, 304, 306, 307
high-aspect-ratio wings, 73, 75
high-speed wings, 73, 74–75, 78 ibises, 25, 80, 82, 123, 159, 181
Hoatzin (Opisthocomus hoatzin), 36, 37, 173 imprinting, 340, 391
hole nesters, 293, 296, 301, 355, 357, 358 inbreeding, 325
Holmes, Richard T., 153–54, 195 incubation: of altricial vs. precocial birds,
homeothermy, 1, 20, 79, 217 338; behavioral adjustments during,
Index

honeyeaters, 36, 108, 117, 118, 135 228–29; brood patch and, 50, 57, 289,
honeyguides, 51, 384, 387 308; brood reduction and, 359; in cold

445

1stPages_B.indd 445 7/22/20 11:59 AM

 climates, 287–88; dissipation of heat kiwis, 50, 51, 80, 82, 178, 292
during, 286–87, 288; energy expen- knee running, 16
ditures during, 62, 282; heat delivery K-T (Cretaceous-Tertiary) boundary, 18
during, 285–86, 287, 388; optimal
temperatures for, 285, 338, 339; paren- Lack, David, 301
tal attentiveness and, 285–86. See also Lake Duck (Oxyura vittata), 284
eggs landings, 67, 71
indeterminate layers, 50, 285, 336–38 landscape ecology, 402–4
Indigo Bunting (Passerina cyanea), 105, larks, 116, 332
168, 169, 268 larynx, 38–39
information center effect, 198, 314 latitudinal gradients, 145–49, 150, 356–57
insulin, 35, 59 Lazuli Bunting (Passerina amoena), 105,
intelligence, 47–48 168, 169
internal coincidence model, 305 Leach’s Storm-petrel (Oceanodroma leucor-
International Commission on Zoological rhoa), 51, 302
Nomenclature, 156 leapfrog migration, 274
International Union for Conservation of legs, 23, 46, 70, 115, 116
Nature (IUCN), 406 leks, 368–70, 372, 387
interspecific territoriality, 196–98, 329 Lesser Snow Goose (Chen caerulescens), 282
intestinal tract, 35–37, 342 LH. See luteinizing hormone
invasive movements, 240 limpkin, 179
irruptive movements, 223, 240, 347 Linnaeus, Carl, 155, 156
islands: biogeographical studies, 131–33, liver, 35, 43
403; bird community patterns, 130–44; lobate feet, 115, 116
equilibrium model and, 131–33, 403; locomotion: bipedalism, 1, 5, 9, 13, 65; knee
generalizations applied to mainland running, 16; quadrupedalism, 1, 4–5, 9.
communities, 142–44; nesting colonies See also flight
on, 313–14; radiation in isolated systems, Loggerhead Shrike (Lanius ludovicianus),
108–11; speciation on, 107–8; spe- 360
cies-area curve and, 130–31, 133, 135–36 long-distance migrants: defined, 240;
IUCN (International Union for Conserva- examples of, 240, 241, 247; humidifi-
tion of Nature), 406 cation of air by, 39; hyperphagia and,
264; management of, 404; pectoral
jacamars, 122, 182 muscles of, 47; stellar cues used by,
jacanas, 115, 116, 289, 373, 374 268
Jamaican Emerald (Mellisuga minima), 292 Long-tailed Manakin (Chiroxiphia linearis),
James, Frances, 15, 400, 402 26
Japanese Quail (Coturnix japonica), 52 loons, 70–71, 181
juncos, 201, 255 loops of Henle, 43, 232–33
lumpers, 86, 157
kagu, 181 lungs, 19, 38–40
keratin, 281, 291 luteinizing hormone (LH), 57, 281, 306
kidneys, 41, 43, 44, 232–33 lyrebirds, 46, 328
kingfishers, 95, 120, 148–49, 150, 182
kinglets, 125, 218 MacArthur, Robert, 93–94, 131
kin selection, 379, 382 MacArthur-Wilson equilibrium model,
Index

Kirtland’s Warbler (Setophaga kirtlandii), 131–33, 403

384, 400, 404 magnetic sensory organs, 56

446

1stPages_B.indd 446 7/22/20 11:59 AM

 Magnificent Frigatebird (Fregata magnifi- and, 74. See also long-distance migrants
cens), 313, 331, 361–62 mimicry, 328–29
male dominance polygyny, 368–71 mixed-species flocks, 205–6, 207
male reproductive system, 282–83 moas, 80–81
Mallard (Anas platyrhynchos), 51, 70, 296, mobbing behavior, 199
297, 304, 390 molecular biology, 163–75; genomic studies,
Mallee Fowl (Leipoa ocellata), 388, 389 172–75; at lower taxonomic levels,
management practices, 275–76, 399–400, 166–68, 169; species comparisons
402–6 through, 157, 163; tree of life project,
manakins, 26, 124, 148, 369, 370, 395 168, 170–73, 171. See also DNA
Manx Shearwater (Puffinus puffinus), 266 molting process, 24–26, 243, 309
marginal value theorem (MVT), 212–13 Monk Parakeet (Myiopsitta monachus), 393
mating behavior: assortative, 324, 325; monogamy: breeding territories and, 311;
birdsong and, 162, 316–17, 324–25; characteristics of, 310; cooperative, 376;
hormonal influences on, 51; migration extra-pair copulations in, 363; genetic,
and, 329–30; territorial, 193. See also 363, 364, 376; with helpers, 378–82;
copulation; courtship behavior; monog- migration habits and, 255; natural
amy; polygamy selection and, 362; nesting colonies
meadowlarks, 103, 151, 168, 218 and, 315; pair-bonding in, 329, 333,
medulla, 49–50, 58 362–63; social, 363–64
megapodes, 285, 291, 388 Monroe, Burt, 165–66
melatonin, 305 morphological adaptations: to cold, 218–20;
Mengel, Robert, 101 for flight, 78; to heat, 228; parasitic
mesites, 173, 179 specialization and, 387; to xeric condi-
metabolism, 59–64, 216 tions, 231
midbrain, 49 morphological convergence, 149, 158
migration, 239–78; age and sex differences Mourning Dove (Zenaida macroura), 360
in, 253, 255–56; altitude flown during, mousebirds, 182
40, 264; annual cycles of, 275, 404; murres, 293, 294, 314
behavioral ecology en route, 264–65; Muscovy Duck (Cairina moschata), 390
climatic factors related to, 252, 259–63; muscular stomach. See gizzard
conservation of migratory birds, 275– muscular system, 19, 44–47
78, 277, 408; defined, 239; destinations Mute Swan (Cygnus olor), 306
for, 252–53, 254; evolution of, 249, 259, mutualisms, 117, 147–48, 235–38, 360, 395
270–75, 273; food habits and, 245–47, MVT (marginal value theorem), 212–13
260, 271–72; geography and habitat
effects on, 247–49, 250; management National Audubon Society, 250, 398
practices and, 275–76, 404–6; mating natural selection: birdsong and, 317, 321,
behavior and, 329–30; mechanics of, 322; clutch size and, 345; defined,
258–70; navigation and orientation 83; foraging behavior and, 188, 207;
in, 265–70; patterns of movement, monogamy and, 362; nest building
249–52; reproductive period and, 309; and, 336; phenotypes and, 164; specia-
route selection for, 258–59; short-dis- tion and, 83–84, 87, 100, 108; system-
tance, 240, 242, 264, 268; site fidelity atic studies and, 164; timing of breed-
and, 243, 256–58, 276; soaring during, ing and, 360. See also evolution
76, 264; timing of, 259–65; trade-offs navigational abilities, 265–70
Index

related to, 270–74, 273; types of move- neck muscles, 46

ment, 240–45, 241–42, 244; wing shape neocortex, 48–49

447

1stPages_B.indd 447 7/22/20 11:59 AM

 neoteny, 81–82 221–22; food storage by, 234; foraging
nervous system, 47–50 behavior of, 217; interspecies varia-
nest building: antipredator devices, 334, tions, 87–88, 89, 92
336; birdsong and, 320; in courtship nutrition. See food
behavior, 330, 333; functions of, 334;
genetic influences on, 162; habitat fac- Oak Titmouse (Baeolophus inornatus), 217
tors in, 334–35; hole nesters, 293, 296, odors, as navigational cues, 270
301, 355, 357, 358; hormonal influences OFMs. See optimal foraging models
on, 306; natural selection and, 336. See Oilbird (Steatornis caripensis), 56
also cavity nesters; nesting colonies olfaction, 49, 51
nesting colonies: costs and benefits of, oocytes, 280–81
314–15, 336; courtship behavior in, 330, optic lobes, 49, 51
332; egg color and, 293, 336; foraging optimal foraging models (OFMs), 187, 188,
behavior in, 198, 315; motivations for, 207–15
312–14; polygyny in, 366; for predator oral cavity, 34
defense, 314–15; territorial behavior in, Orians, Gordon, 365
313–15 orientational abilities, 265–70
nestlings: altricial vs. precocial, 299–301, Oring, Lewis, 362
339, 342; factors affecting growth rate orioles, 105, 336
of, 301–3; feeding, 234, 311, 339–42, ornithological societies, 10, 86, 88, 177,
343; mortality rates among, 214, 302; 398–99
parental care of, 338–44; sensitive ornithology, defined, 1. See also birds
periods for, 326; survivorship with one ornithurines, 16–18, 17
parent, 362 ostriches: bare skin on, 23; egg size of, 292;
New Caledonian Crow (Corvus moneduloi- feather structure, 22; flightless, 79, 80,
des), 48 82; foot design of, 116; foraging behav-
Newcastle disease, 393 ior of, 200; intestinal tract of, 37; non-
nictitating membrane, 52 territorial group breeding by, 376–77;
nidicolous birds. See altricial birds reproductive organs of, 284; salt glands
nidifugous birds. See precocial birds in, 232; taxonomic classification, 178
nocturnal migrants, 263, 267–70 Ostrum, John, 13
nomadism, 243, 252, 276 ovaries, 280, 285, 289, 308, 336
nonterritorial group breeding, 376–77 Ovenbird (Seiurus aurocapilla), 170, 172,
nonvocal sounds, 329 191, 193, 276
Northern Harrier (Circus cyaneus), 77 oviduct, 280, 281
Northern Mockingbird (Mimus polyglottos), ovulation, 281, 304, 306–7, 330
86, 320, 328 owls: bills of, 117, 119; brood patch of, 289;
Northern Parula (Setophaga americana), ecological impact of, 395; egg laying
243 by, 284; eyes of, 53, 54; feathers of, 23;
Northern Pintail (Anas acuta), 88 fledgling period in, 303; flightless, 81;
Northern Wheatear (Oenanthe oenanthe), foraging behavior of, 217, 247; gular
257 flutter utilized by, 230; hearing ability
Northwestern Crow (Corvus caurinus), 215 of, 55, 56, 57; incubation of eggs, 288;
nuclear species, 206 pellet formation and regurgitation in,
numerical taxonomy, 160 36; rotation of head by, 33, 56; semial-
nuptial plumage, 24–25 tricial, 299; taxonomic classification,
Index

nuthatches: bills of, 121; character displace- 182; territorial behavior of, 193, 195;
ment and, 98, 99; in cold climates, 218, timing of breeding by, 360

448

1stPages_B.indd 448 7/22/20 11:59 AM

 oxytocin, 57, 307 pet birds, 392–94
Peters, James L., 170
Painted Bunting (Passerina ciris), 26, 244 petrels, 51, 227, 302
pair-bonding, 317, 327–33, 331, 362–63, 374, phalaropes, 289, 308, 375
391 pheasants, 116, 347, 396
paleontology, avian, 2–8, 10, 15 phenetic taxonomy, 160
paleornithology, 3, 80 phenotypes, 84, 158, 161, 164
palmate feet, 115, 116 Philadelphia Vireo (Vireo philadelphicus),
pamprodactyl feet, 115 197, 329
pancreas, 35, 59 philopatry, 243, 256
panting, 229–31, 287 phoebes, 246, 334, 364
Papuan Frogmouth (Podargus papuensis), phorusrhacids, 81, 82
231 photoperiods: in clock-shift experiments,
parakeets, 393 267; heat production and, 223; hor-
parapatric species, 100 monal control triggered by, 227; mech-
parasitism, 383–88 anism for tracking, 49; reproduction
parathyroid glands, 59 and, 304–6, 360; in timing of migra-
parrots: artificial nests for, 405; bills of, 124; tion, 263–64
copulation among, 284; flightless, 80; photorefractoriness, 308–9
intelligence of, 48; nonnative species, phylogenetic species concept (PSC), 176–77
393; in pet trade, 394; song variation physiological adaptations: to cold, 222–27;
among, 319; taste buds among, 51; for flight, 258; to heat, 228–30; to xeric
taxonomic classification, 183 conditions, 231–33
partial migrants, 240 physiology. See anatomy and physiology
Partners in Flight program, 275, 408 Pied Flycatcher (Ficedula hypoleuca), 341,
Pearlyeyed Thrasher (Margarops fuscatus), 366
405 pigeons: brain structure of, 49; brood
pecten, 52 patch of, 289; cooling strategies of,
pectoralis muscle, 44–45, 46 231; domesticated, 390, 393; eyes
Pelagornis sandersi, 79 of, 54; flightless, 80; guild structure
pelicans: bills of, 120; black wing tips for, 133–34; hearing ability of, 55–56;
among, 25; feeding of nestlings by, 343; intelligence of, 48; milk secreted by,
foraging behavior of, 198; gular flutter 36; navigation and orientation among,
utilized by, 230; gular pouch of, 118; 265–69; nest building by, 335; prolactin
soaring ability of, 79; taxonomic classi- levels in, 308; reproduction in, 309;
fication, 181 taste buds in, 51; taxonomic classifica-
penguins: communal roosting by, 222; tion, 173, 179
esophagus among, 36; fat storage by, pineal gland, 304, 305
63–64; feather structure, 22; flightless, Pine Grosbeak (Pinicola enucleator), 34
79–80; taxonomic classification, 181; Pine Warbler (Setophaga pinus), 240, 242
territorial behavior of, 193; tracking Pinyon Jay (Gymnorhinus cyanocephalus),
mechanisms for, 405 235, 237, 238, 360
penis, 51, 284 pipping, 296–97
pennaceous feathers, 20, 22 pittas, 121, 151–52
perching birds, 46, 115, 163, 183–86 pituitary gland, 56–58, 281, 289, 307
peripheral nervous system (PNS), 48 Pleistocene glaciation, 101–5, 104
Index

permanent residents, 240, 271–72 plumage: in flocking species, 204; as heat

Perrins, Chris, 302–3 barrier, 228; interspecies variations,

449

1stPages_B.indd 449 7/22/20 11:59 AM

 87, 88, 100; iridescent, 15, 26; nomen- protein electrophoresis, 163–64
clature for, 24–25; of pet birds, 392; Prum, Richard, 10, 13, 15
polygyny and, 370–72; protection of, PSC (phylogenetic species concept), 176–77
22; status signaling and, 202–4; touch pseudosuchian thecodont hypothesis, 9–13,
receptors on, 50. See also feathers 16
plumulaceous feathers, 20 pterylae, 22, 23
PNS (peripheral nervous system), 48 Puerto Rican Parrot (Amazona vittata), 393,
pollinators, 117, 147–48, 265, 395 405
polyandry: cooperative, 376, 380–82; Puerto Rican Tody (Todus mexicanus), 86,
defined, 363; migration habits and, 255; 122
prevalence of, 372; sequential, 363, 373, puffbirds, 182
374, 376; sexual dimorphism and, 375; Pygmy Nuthatch (Sitta pygmaea), 221–22
simultaneous, 363, 374
polygamy: cooperative, 380, 381; environ- quadrupedalism, 1, 4–5, 9
mental potential for, 362–66, 370, 373, quail, 52, 396, 400
375, 388; rapid multiple clutch, 374. See
also polyandry; polygyny rachis, 20, 22
polygyny: birdsong and, 321; brood par- radiation, 108–25; adaptations resulting
asitism and, 387; cooperative, 376; from, 114–25; evolutionary patterns
defined, 363; delayed maturation and, of, 16–18, 111–14; in isolated island
203, 371; evolution of, 191, 365–70; systems, 108–11; of terrestrial animals,
female defense, 369; genetic, 363, 364; 2–5, 4. See also speciation
male dominance, 368–71; migration radio-tracking devices, 278, 405
habits and, 255; in nesting colonies, rails, 80, 82, 179
366; resource defense, 366, 368–70; rapid multiple clutch polygamy, 374
sequential, 363; sexual selection in, raptors: ecosystem role of, 395; extra-pair
370–72; simultaneous, 363; territorial young among, 364; feeding of nest-
harem, 368, 376 lings by, 341; feet of, 115, 116, 124;
polygyny threshold model, 365–66 incubation of eggs, 338, 359; irruptive
population fluctuation, 346–47 movements by, 240; migration of, 247,
population regulation, 195–98, 347–50 255; salt glands in, 232
postural adjustments, 61, 220–22, 221, ratites, 79–82, 284, 376
228–29 reciprocal altruism, 199
Pourtless, John, 15 rectrices. See tail feathers
powder down feathers, 21, 22 Red-billed Quelea Finch (Quelea quelea),
powered flight, 68–70 304
precocial birds: brood parasitism and, 383; Red-breasted Nuthatch (Sitta canadensis),
characteristics upon hatching, 298–99; 217
clutch size and, 358; digestive system Red Data Book (IUCN), 406
in, 302; egg size and structure of, 290, Red-eyed Vireo (Vireo olivaceus), 197, 329
292, 299; embryonic development of, Red Junglefowl (Gallus gallus), 390–92, 391
296, 299; imprinting among, 340; redpolls, 220, 227
incubation of, 338; nestling period in, Redshank (Tringa totanus), 209, 210
300–301, 339, 342; polygyny and, 366, Red-winged Blackbird (Agelaius phoeni-
368; prolactin levels and, 308 ceus), 84, 162, 191, 197, 365
predatory birds, 350, 360, 395, 405 remiges. See wing feathers
Index

progesterone, 306–8 reproduction, 279–389; age at first repro-

prolactin, 57, 58, 289, 305–8 duction, 350; birdsong and, 316–29,

450

1stPages_B.indd 450 7/22/20 11:59 AM

 323; coordination with annual cycle colubris), 258, 259, 265
events, 309; in domesticated species, Ruff (Philomachus pugnax), 371–72
306, 391; embryonic development, Ruffed Grouse (Bonasa umbellus), 220, 342
285, 286, 294–97; female reproduc- Rufous-collared Sparrow (Zonotrichia cap-
tive system, 280–82; fertilization in, ensis), 322, 324
281–84, 294, 330, 363, 368; hormonal
control of, 281, 306–8; male reproduc- salivary glands, 34, 36
tive system, 282–83; mate acquisition salt glands, 51, 232
for, 162, 193, 260, 316–17, 324–25; sandgrouse, 23, 173, 179, 231–32, 338
photoperiod control of, 304–6, 360; sandpipers: bills of, 50; brood patch of,
population effects of, 346–50; purposes 289; hyperphagia and, 264; migra-
of, 279; sex determination system in, tion of, 249, 252, 255, 260; polyandry
284; termination of, 308–9; territories among, 372–74; precocial, 299; territo-
and spacing during, 311–15; timing of rial behavior of, 193
reproductive events, 303–9. See also Savannah Sparrow (Passerculus sandwichen-
breeding; copulation; courtship behav- sis), 233, 234, 270
ior; eggs; mating behavior; nest build- screamers, 22, 178
ing; nestlings; reproductive isolation; seabirds: brood patch of, 289; clutch size
reproductive success of, 355; courtship behavior of, 330,
reproductive isolation: anatomical factors 332–33; dynamic soaring by, 75; egg
in, 284; birdsong and, 317, 318; defined, laying by, 284; extra-pair young among,
85; dynamics of, 88, 90–91; Pleisto- 364; fledgling period in, 344; foraging
cene glaciation and, 101–3; in specia- behavior of, 191; incubation of eggs,
tion process, 100–101, 126 338; navigational ability of, 266; nest-
reproductive success: aggressive neglect ing colonies of, 315; reproduction in,
and, 198; brood parasitism and, 384; 345, 350; timing of breeding by, 362
factors impacting, 350, 363; fat reserves search image, 211, 335
and, 282; foraging behavior and, 208; seed dispersal, 235, 236, 395
group breeding and, 380; migration semialtricial birds, 298, 299, 339
and, 260, 271, 272, 274; polygyny and, semipalmate feet, 115, 116
366 semiplumes, 21, 22
reproductive systems, 280–83 semiprecocial birds, 298, 299, 339
reptiles, in bird ancestry, 3–6 sensory organs: ears, 55–56, 57, 159; eyes,
resource defense polygyny, 366, 368–70 26–27, 51–55, 53; magnetic, 56; smell,
respiratory system, 38–40, 42 49, 51; taste, 34, 51; touch, 50–51
rete, 227, 231 sequential polyandry, 363, 373, 374, 376
retina, 51, 52, 54 sequential polygyny, 363
reverse sexual dimorphism, 375 Sereno, Paul, 9
rheas, 80, 178, 297, 376 seriemas, 173, 183
Ricklefs, Robert, 107, 301–3 sex determination system, 284
Ring-necked Pheasant (Phasianus colchi- sexual dimorphism, 205, 333, 338, 370, 375,
cus), 347 387
roadrunners, 116, 222 sexual reproduction. See reproduction
robins, 34, 246, 347, 360 sexual selection, 13, 321, 370–72
Rohwer, Sievert, 204–5 Shiny Cowbird (Molothrus bonariensis), 384
Rosy Finch (Leucosticte arctoa), 34, 92, 100 shorebirds: brood patch of, 289; clutch
Index

route selection for migration, 258–59 size of, 354; digestive system of, 37;
Ruby-throated Hummingbird (Archilochus extra-pair young among, 364; fledg-

451

1stPages_B.indd 451 7/22/20 11:59 AM

 ling period in, 344; foraging behavior 327; song variation among, 320, 322,
of, 201–2; migration of, 257, 258; 324; subspeciation among, 88; terri-
polygamy among, 372, 374; taxonomic torial behavior of, 191, 192; timing of
classification, 173, 180–81; territorial breeding by, 361; in xeric conditions,
behavior of, 193, 201; transitory, 18; 233, 234
water transport by, 231–32 speciation, 83–108; allopatric, 101, 105, 108;
short-distance migrants, 240, 242, 264, 268 competition and, 91–93, 97–100, 127;
shrikes, 117, 119, 234, 328, 360 continental drift and, 90, 111–14; diver-
Sibley, Charles, 164–66, 167, 170 sity determined by rates of, 126–27;
sight. See eyes ecological isolation and, 92–97,
simultaneous polyandry, 363, 374 100–103, 126–28, 138; on islands,
simultaneous polygyny, 363 107–8; mechanisms of, 100–108; natu-
site dominance, 193, 202–4, 271–74, 273, ral selection and, 83–84, 87, 100, 108;
364 Pleistocene glaciation and, 101–5, 104;
site fidelity, 243, 256–58, 276 subspeciation, 87–88, 89–90, 101; in
skeletal system, 19, 30–33, 32 tropical America, 105–7. See also diver-
skimmers, 118, 120 sity; radiation; reproductive isolation
skin, 22–23, 27–29, 50 species: attendant, 206; biological con-
slotted high-lift wings, 73, 75–76 cept, 85–86, 157, 163, 176–77; conver-
smell, 49, 51 gent, 82, 149, 151–52; defined, 85, 87;
snipes, 50, 375 nomenclature for, 85–86, 88; nuclear,
soaring, 45, 75–79, 264 206; parapatric, 100; phylogenetic con-
Sociable Weaver (Philetairus socius), 220 cept, 176–77; variation within, 87–88,
social monogamy, 363–64 89–90. See also speciation; specific
solar cues, 267–68 species
songbirds: intelligence of, 47; migration species-area curve, 130–31, 133, 135–36
of, 243, 258; molting process of, 24; spermatozoa, 282–84
syrinx of, 39; wing shape of, 74. See also spinal cord, 48–50
birdsong splitters, 86, 157
Song Sparrow (Melospiza melodia), 88, 191, Spotted Sandpiper (Actitis macularia), 255,
192, 218 373, 374
Sooty Tern (Onychoprion fuscatus), 362 stabilizing selection, 83, 84
Southwest Pacific islands: bird community stalls, 66–67, 68, 70–71
patterns, 97, 133–34, 135; generaliza- stapes, 159
tions applied to mainland communi- starlings, 51, 208, 211–15, 212, 265–66, 347
ties, 144; guild designations in, 133–34, static soaring, 76–77, 79
142; seed size on, 141; species-area status signaling, 202–5
curve for, 131, 133 Steadman, David, 110
sparrows: in cold climates, 218, 220; domi- stellar cues, 268
nance interactions among, 204–5; egg Stephens Island Wren (Traversia lyalli), 80
production in, 281–82; energy expendi- stomach, 20, 35–37, 59
tures, 62, 63; fledgling period in, 303; storks: bills of, 50, 123; flightless, 81; nav-
flying altitude of, 40; foraging behavior igation and orientation among, 266;
of, 187; heart size among, 42; migra- soaring ability of, 76, 79; taxonomic
tion of, 253; navigation cues utilized by, classification, 181; urohydrosis exhib-
270; in photoperiod studies, 305, 308; ited by, 229
Index

reproductive organs of, 283; scientific summer residents, 240, 274

names, 86; sensitive periods for, 326, sunbirds, 117, 118, 125, 191, 194, 370

452

1stPages_B.indd 452 7/22/20 11:59 AM

 sunbitterns, 173, 181 Tawny Owl (Strix aluco), 193
super-high-speed wings, 73, 76–78 taxon cycle, 107
supplemental plumage, 25 taxonomy: birds of the world classification,
supracoracoideus muscle, 44–45, 46 177–86; controversy regarding, 86–87;
surface-area-to-volume ratios, 216–18, 220, evolution of, 156–57; lumpers vs.
228, 253, 334 splitters in, 86, 157; molecular biology
Swainson’s Hawk (Buteo swainsonii), 247, at low levels of, 166–68, 169; nomen-
249 clature in, 85–86, 88, 156; numerical
swallows: bills of, 122; brood patch and, (phenetic), 160; objectives of, 155; struc-
289; clutch size of, 354–55; extra-pair tural format for, 155–56; the tapestry
young among, 364; migration of, 253, (Sibley), 166, 170; tree of life project,
258; navigational ability of, 266 168, 170–73, 171. See also systematics
swans: breeding in, 306; egg laying by, 284; teeth, evolution of, 11
feathers of, 29; flying ability of, 64, Teratornithidae, 79
79; flying altitude of, 264; pair-bonds Terborgh, John, 97, 152–53, 275
among, 329; taxonomic classification, termination of reproduction, 308–9
178 terns, 247, 299, 314, 336, 362
swifts: bills of, 122; clutch size of, 354; cop- territorial behavior: acquisition and
ulation among, 333–34; echolocation defense, 193–95, 202–3; birdsong and,
and, 56; foot design of, 115; foraging 316, 320; breeding territories, 195,
behavior of, 191; geolocator studies 311–12, 316, 377–83; costs and benefits
of, 278; intestinal tract among, 37; of, 188–91; evolution of, 188, 189–90,
migration of, 253; pellet formation and 312; interspecific, 196–98, 329; in leks,
regurgitation in, 36; torpor utilized by, 368–69; of mixed-species flocks, 206,
224; wing shape of, 76 207; in nesting colonies, 313–15; popu-
syndactyl feet, 115, 116 lation regulation and, 195–98; resource
syrinx, 38, 39, 162–63, 329 distribution and, 188–91, 311; size and
systematics, 155–77; behavioral and ecolog- shape of territories, 191–93, 192; status
ical characteristics in, 162; challenges signaling and, 202–3
associated with, 157–58; cladistic territorial harem polygyny, 368, 376
approach to, 160–61; electrophoretic testes, 282, 284, 304, 305, 364
techniques in, 163–64; evolution of, testosterone, 306, 308
156–57; genomic approaches to, 172–75; thalamus, 49
molecular biology and, 157, 163–75, thecodonts, 4, 5–6, 9–13, 15, 16
169, 171, 176; morphological and thermoneutral zone (TNZ), 61–62, 216
physiological traits in, 162–63; numer- theropod hypothesis, 9–13, 15, 16
ical approach to, 160; objectives of, Thorpe, William, 325–26
155, 157; phylogenetic species concept thrashers, 328, 405
in, 176–77; traditional approaches to, thymus, 59
158–60. See also taxonomy thyroid gland, 58
thyroid-stimulating hormone (TSH), 57, 58
tail, 46, 71, 123 thyroxin, 57–58
tail feathers, 29, 31, 46, 278 time, ecological isolation by, 96–97
takeoffs, 45, 67, 70–71 timing of migration, 259–65
tapestry (Sibley), 166, 170 tinamous, 159, 173, 284, 294, 376
Tasmanian Native Hen (Gallinula mortie- Tinbergen, Joost, 214
Index

rii), 382 tip vortex, 72, 74

taste, 34, 51 titmice, 95, 187, 217, 234

453

1stPages_B.indd 453 7/22/20 11:59 AM

 TNZ (thermoneutral zone), 61–62, 216 vagina, 281, 284, 307
tongue, 33–34, 50 vasotocin, 57, 233, 307
topographic cues, 269–70 Velociraptor, 9, 12
torpor, 63, 79, 217, 224–26 Verner, Jared, 196, 365
totipalmate feet, 115, 116 vireos, 197, 253, 329, 384
toucans, 122, 124, 182–83 vision. See eyes
touch, 50–51 vultures: bare skin on, 23; basking behavior
trachea, 38–40 of, 222; ecosystem role of, 395; fat stor-
tracking mechanisms, 405 age by, 217; flightless, 81; landings by,
transitory shorebirds, 18 71; migration of, 258–59; smell ability
tree of life project, 168, 170–73, 171 in, 51; static soaring by, 76; taxonomic
Tree Swallow (Tachycineta bicolor), 364 classification, 181–82; tool use among,
Tricolored Blackbird (Agelaius tricolor), 162 215; urohydrosis exhibited by, 229
trogons, 182
trophic convergence, 145 wagtails, 210, 386
tropical areas: distribution of, 248–49; Wallace, Alfred Russel, 156
group breeding in, 377; habitat separa- Warbler Finch (Certhidea olivacea), 109
tion in, 94, 97, 147; island bird com- warblers: bills of, 246; brood parasitism
munity patterns, 140–41, 142; migra- and, 384; convergence among, 151;
tion to, 250–51, 262, 272; mutualisms copulation among, 284; ecological
within, 147–48; nestling growth rates isolation among, 93–94, 97; foraging
in, 302; population stability in, 346, behavior of, 96; habitat requirements
348, 349; resource availability in, 147, for, 400, 401, 404; hybridization
148–49; speciation in, 105–7; territorial among, 102; hyperphagia and, 264;
behavior in, 190, 191, 312; timing of migration of, 240–43, 241–42, 253,
breeding in, 361; trophic comparisons 258–59, 262, 274, 276; in tree of life
of, 145 project, 170, 172
tropicbirds, 173, 181 warm-bloodedness. See homeothermy
trumpeters, 179 warning calls, 199
TSH (thyroid-stimulating hormone), 57, 58 water shortages, 231–34
tube-nosed swimmers, 181 waves of migrants, 261
Tufted Titmouse (Baeolophus bicolor), 95 webbed feet, 115, 116, 228
Tundra Swan (Cygnus columbianus), 29 Western Grebe (Aechmophorus occidentalis),
turacos, 173, 179 330–32, 331
turkeys: blood pressure in, 41; domesti- Western Kingbird (Tyrannus verticalis), 245
cated, 390; economic value of, 393; Western Scrub-Jay (Aphelocoma californica),
heart rate of, 42; prolactin levels in, 378
308; weight of, 392 West Indies: bird community patterns,
Turkey Vulture (Cathartes aura), 51, 217, 135–40; generalizations applied to
222, 258–59 mainland communities, 142–44;
Tyrannosaurus rex, 5, 9, 11 guild designations in, 136–39, 142,
143; migrations to, 252, 253, 259, 274,
undulating flight, 78 275; seed size in, 140, 141; species-area
uric acid, 44, 232–33, 295 curve for, 130–31, 135–36; taxon cycle
urinary system, 43–44 and, 107; timing of breeding in, 361;
urohydrosis, 229 vegetation types in, 135, 136
Index

wheatears, 257, 259

454

1stPages_B.indd 454 7/22/20 11:59 AM

 White-breasted Nuthatch (Sitta carolinen- woodcocks, 53, 54
sis), 87–88, 89, 92, 217, 218 woodhoopoes, 159, 376, 377
White-crowned Sparrow (Zonotrichia leuco- Woodpecker Finch (Camarhynchus palli-
phrys), 308, 324, 326, 327 dus), 215
White Tern (Gygis alba), 336 woodpeckers: bills of, 121; brood patch of,
White-throated Sparrow (Zonotrichia albi- 289; in cold climates, 218; ecological
collis), 305, 320 isolation among, 97; embryonic devel-
White Wagtail (Motacilla alba), 210 opment of, 296; food storage by, 234,
White-winged Crossbill (Loxia leucoptera), 235, 238; group breeding among, 377,
107 380; nonvocal sounds of, 329; taxo-
White-winged Dove (Zenaida asiatica), 287, nomic classification, 182–83; tongue
288 of, 33, 34, 50; undulating flight by, 78;
Whooper Swan (Cygnus cygnus), 64 wing shape of, 74
Whooping Crane (Grus americana), 39 Wood Stork (Mycteria americana), 50, 227
Wild Turkey (Meleagris gallopavo), 390 Woolfenden, Glen, 378
Willson, Mary, 365 wrens: breeding systems among, 382;
Wilson, E. O., 131 clutch size of, 345, 355; egg size of, 292;
Wilson Ornithological Society, 399 flightless, 80; incubation of eggs, 286;
wing feathers, 24, 25, 29 mating behavior of, 329; song variation
wing loading, 72–74, 73, 77–79 among, 323, 328
wings: adaptations in, 123–24; aerodynam-
ics and, 72, 73; angle of attack, 66, xeric environments, 231–34
67, 70, 71; camber of, 66–67, 74–76;
categories of, 72–78, 73; evolution of, Yellow-eyed Junco (Junco phaeonotus), 201
1, 12–13; of flightless birds, 81; gliding Yellow-headed Blackbird (Xanthocephalus
actions of, 65–68; in landings, 67, 71; xanthocephalus), 86, 162, 197
musculature of, 44–45, 46; in powered Yellow-shouldered Blackbird (Agelaius xan-
flight, 69–70; structure of, 29, 31; in thomus), 384
takeoffs, 67, 70–71. See also flight yolk, 280–82, 290–91, 295, 296, 299
winter plumage, 25
winter residents, 240, 250, 252, 260–61, Zebra Finch (Poephila guttata), 219–20
272–74, 361 Zugunruhe, 263, 268
wishbone. See furcula zygodactyl feet, 115, 116 Index

455

1stPages_B.indd 455 7/22/20 11:59 AM