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Infectious Diseases in Primates
Oxford Series in Ecology and Evolution
Edited by Paul H. Harvey and Robert M. May
The Comparative Method in Evolutionary Biology
Paul H. Harvey and Mark D. Pagel
The Causes of Molecular Evolution
John H. Gillespie
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Natural Selection: Domains, Levels, and Challenges
George C. Williams
Behaviour and Social Evolution of Wasps:
The Communal Aggregation Hypothesis
Yosiaki Itô
Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology
Eric L. Charnov
Quantitative Ecology and the Brown Trout
J. M. Elliott
Sexual Selection and the Barn Swallow
Anders Pape Møller
Ecology and Evolution in Anoxic Worlds
Tom Fenchel and Bland J. Finlay
Anolis Lizards of the Caribbean:
Ecology, Evolution, and Plate Tectonics
Jonathan Roughgarden
From Individual Behaviour to Population Ecology
William J. Sutherland
Evolution of Social Insect Colonies: Sex Allocation and Kin Selection
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Natural Hybridization and Evolution
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Evolution of Sibling Rivalry
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Asymmetry, Developmental Stability, and Evolution
Anders Pape Møller and John P. Swaddle
Metapopulation Ecology
Ilkka Hanski
Dynamic State Variable Models in Ecology: Methods and Applications
Colin W. Clark and Marc Mangel
The Origin, Expansion, and Demise of Plant Species
Donald A. Levin
The Spatial and Temporal Dynamics of Host-Parasitoid Interactions
Michael P. Hassell
The Ecology of Adaptive Radiation
Dolph Schluter
Parasites and the Behavior of Animals
Janice Moore
Evolutionary Ecology of Birds: Life Histories, Mating Systems and Extinction
Peter Bennett and Ian Owens
The Role of Chromosomal Change in Plant Evolution
Donald A. Levin
Living in Groups
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Anne E. Magurran
Infectious Diseases in Primates: Behavior, Ecology and Evolution
Charles L. Nunn and Sonia Altizer
Infectious Diseases in
Primates
Behavior, Ecology and Evolution

CHARLES L. NUNN
Max Planck Institute for Evolutionary Anthropology, Germany and
University of California, USA

SONIA ALTIZER
University of Georgia, USA

1
1
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Nunn, Charles L.
Infectious Diseases in Primates : Behavior, Ecology and Evolution /
Charles L. Nunn, Sonia M. Altizer.
p. cm.
ISBN-13: 978–0–19–856585–7 (alk. paper)
ISBN-13: 978–0–19–856584–0 (alk. paper)
1. Primates—Diseases. 2. Communicable diseases.
3. Communicable diseases—Environmental aspects.
I. Altizer, Sonia M. II. Title.
RC112.N85 2006
616.9—dc22 2006000425
Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India
Printed in Great Britain
on acid-free paper by
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10 9 8 7 6 5 4 3 2 1
Preface

During the past 25 years, primatologists have remarkably advanced knowledge of

primate behavior, ecology, and evolution, providing a deeper understanding of factors
driving variation in primate social systems and expanding our perspectives on
human evolution. Research in disease ecology over the past several decades has
simultaneously identified a number of core principles through a combination of
theory and data analysis. Despite this progress—and perhaps even because of it—
several gaps have become increasingly obvious. From the perspective of primate
biology, we know surprisingly little about the role of infectious diseases in the lives
of nonhuman primates in their natural environments. From an epidemiological per-
spective, important questions involve the role of variation in host social interactions
and behavior on the dynamics of infectious diseases.
As a well-studied clade of social animals, primates offer the opportunity to explore
how host behavior and ecology can alter the spread of infectious diseases, and to
examine the hypothesis that parasites are a potent selective force on host sociality.
Addressing these issues requires combining ecological and evolutionary perspectives
together with details on primate traits that are likely to influence disease risk and
characteristics of the parasites themselves. The idea that parasites are important in
the lives of social animals such as primates is not a new one. Yet common wisdom
and new hypotheses have yet to be explored in a synthetic framework that examines
variation among individuals, groups, populations, and even species. With this in
mind, our goal in writing this book is to identify key questions in a framework that
integrates existing knowledge of host–parasite interactions with what we know
about primate sociality and behavior, while also examining the implications of this
knowledge for primate conservation and understanding of human evolution.
We are deeply indebted to Janis Antonovics, Colin Chapman, and Bill Freeland,
who gave generously of their time reviewing chapters and provided excellent feedback
that greatly improved the first draft of the manuscript. We also recognize Janis for
detailed comments on all chapters, and for training us earlier in our careers in the
fundamentals of evolutionary biology and inspiring us to study the complex interac-
tions between hosts and parasites. We thank Ian Sherman, Paul Harvey, and Bob May
for being open to the ideas presented in this book and for encouraging us to pursue
them. Pete Richerson, Tim Caro, Monique Borgerhoff Mulder, Christie Henry,
vi • Preface

Michael Pereira, and Michael Sanderson generously gave advice and additional
encouragement to pursue the book project.
Several graduate students and postdoctoral researchers at Emory University and
the University of California at Berkeley provided important comments and critiques
of chapters. At UC Berkeley, we wish to acknowledge students in the “primate disease
seminar,” including Paul Cross, Sadie Ryan, Andrew Ritchie, Mariah Hopkins, Mike
Wasserman, Adrian Dokey, Jessie Standish, and Denise Bonilla. At Emory, we thank
Roman Biek, Jaap de Roode, Kristin Harper, Catherine Bradley, Liz Harp, Elizabeth
Lindsey, and Nick Vitone. Students and researchers at other institutions provided
crucial comments leading to reformulation or revision of several chapters. For this,
we thank Michael Huffman, Matt Bonds, Britta Mueller, Barbara Fruth, Leslie
Knapp, and Pete Thrall.
Members of the working groups that we co-organized at the National Center for
Ecological Analysis and Synthesis (NCEAS) and Conservation International provided
helpful feedback at many stages, and with their support and encouragement, we
pursued a number of new and exciting projects, with many of the completed research
projects described in this book. We thank in particular John Gittleman, Amy
Pedersen, Andrew Cunningham, Andy Dobson, Pete Thrall, Janis Antonovics, Kate
Jones, Wes Sechrest, Mary Poss, Vanessa Ezenwa, Peter Daszak, and Patrik Lindenfors.
All of these individuals gave their time to two or more meetings of the working
groups, and they played integral roles in developing projects within these groups.
We thank our colleagues who graciously volunteered photographs or advice on
images, including Dawn Kitchen, Ken Glander, Frances White, Alan Dixson,
Dewald Keet, Craig Packer, Katharine Milton, Britta Müller, Brian Byrd, Joyce
Parga, Kerstin Mätz-Rensing, AnaPatricia Garcia, Michael Huffman, Zhang Peng,
Matt Bonds, Kate Jones, Joost Philippa, Catherine Bradley, Martha Robbins, Vanessa
Ezenwa, Peter Kappeler, Ulrike Walbaum and Roland Regoes. Noel Rowe deserves
particular mention for his assistance with finding “just the right image,” including
photos for the front and back cover. Peter Walsh kindly provided unpublished
manuscripts. Special recognition goes to Liz Harp and Laura Gold who helped
extensively in locating photographs and organizing images for several of the chapters,
and Joann Chang and Corine Graham for locating articles, obtaining permission to
use figures, and organizing references. Anja Herb, Claudia Nebel and Claudia Feige
provided help compiling the completed manuscript.
Deep thanks are extended to Sheila Patek and Andy Davis. Sheila provided the
initial encouragement to pursue this book project, and patiently provided moral support
during the book-writing project. She also provided extensive feedback on topics to
cover, advice on proposal preparation, and comments on early versions of the first
chapters. Andy assisted with extensive proofing of the manuscript, provided biblio-
graphic support, and inspired revisions of multiple chapters. Andy also supplied
patience and continued support during the final stages of writing and revisions.
Charlie also wishes to thank his parents, John and Janet Nunn, and Dorothy
McIntyre, for providing a learning environment, education, and support that ultimately
made this work possible. Ken Korey at Dartmouth College taught Charlie about
 Preface • vii

evolution and revealed the pleasures of academic pursuits. Carel van Schaik introduced
Charlie to primate socioecology, changed his career path toward behavioral evolution,
and inspired him to push the boundaries of our knowledge about primate behavior and
ecology. Sonia thanks her parents, Chris and Jim, for encouraging writing, creativity,
and academic scholarship, and her Aunt Carole who cultivated an interest in science
and nature.
In terms of financial and research support, the authors acknowledge the National
Science Foundation (#DEB-0212096), National Center for Ecological Synthesis
and Analysis, Conservation International, the University of California (Davis and
Berkeley), and Emory University. More recently, we are grateful to the Max Planck
Institute for Evolutionary Anthropology and the Institute of Ecology at the University
of Georgia for opportunities to extend our research in new directions by providing
resources and a dynamic, collaborative environment. We appreciate the support that
has been extended to us, and we look forward to developing collaborations with new
colleagues.
Charlie Nunn and Sonia Altizer
October 14, 2005
This page intentionally left blank
Contents

1 Questions, terminology, and underlying principles 1

1.1 Introduction 1
1.2 Essential terminology: parasite, disease, and disease risk 3
1.2.1 What is a parasite? 3
1.2.2 Parasite and disease 3
1.2.3 What is disease risk and how is it measured? 5
1.3 Ecological drivers of primate sociality 8
1.3.1 Between-group resource competition 9
1.3.2 Predation and within-group competition 9
1.3.3 Inter-sexual conflict 10
1.3.4 Infectious disease 10
1.4 Fitness consequences of parasites in wild primate populations 14
1.5 Organizational layout of this book 20

2 Diversity and characteristics of primate parasites 22

2.1 Introduction 22
2.2 Taxonomic diversity of parasites from wild primates 26
2.2.1 Viruses 29
2.2.2 Bacteria 33
2.2.3 Fungi 34
2.2.4 Protozoa 35
2.2.5 Helminths 37
2.2.6 Arthropods 40
2.3 Strategies for parasite transmission 42
2.4 Host specificity and “multi-host” parasites 45
2.5 Virulence: negative effects of parasites on their hosts 48
2.6 Parasite transmission and manipulation of host behavior 52
2.6.1 Causes and consequences of altered behavior 54
2.6.2 Manipulation of primate hosts 54
2.7 Summary and synthesis 55
x • Contents

3 Primate socioecology and disease

risk: predictions and rationale 57

3.1 Introduction 57
3.2 Background concepts 61
3.2.1 Encounter and infection probability 61
3.2.2 Formulating hypotheses at individual and comparative levels 64
3.3 Host traits and disease risk 65
3.3.1 Body mass, life history, and individual age 65
3.3.2 Host population size and density 71
3.3.3 Social organization, group size, and dominance rank 74
3.3.4 Reproduction, mating behavior, and sex differences 80
3.3.5 Ranging behavior, substrate use, and diet 86
3.3.6 Environmental factors and seasonality 92
3.4 Summary and synthesis 95

4 Host–parasite dynamics and

epidemiological principles 98

4.1 Introduction 98
4.1.1 An historical perspective 98
4.1.2 Basic terminology and measures of infection 101
4.2 Analytical models of disease spread 103
4.2.1 Microparasites and compartment models 106
4.2.2 Macroparasite models 115
4.3 The role of parasites in regulating host populations 117
4.3.1 Theoretical predictions 117
4.3.2 Regulation in experimental and natural populations 119
4.4 Heterogeneities and dynamical complexities 122
4.4.1 Spatial heterogeneity: landscape features and
metapopulation dynamics 122
4.4.2 Host social system 123
4.4.3 Multi-host dynamics 128
4.5 Summary and synthesis 132

5 Host defenses: the immune system and

behavioral counterstrategies 134

5.1 Introduction 134

5.2 Responding to infections: strategies for parasite removal 135
5.2.1 Immune defenses 135
5.2.2 Physiological responses and sickness behaviors 148
5.2.3 Grooming as a means of parasite removal 150
5.2.4 Medicinal plant use 155
5.3 Preventing infections: strategies for parasite avoidance 159
5.3.1 Habitat use and ranging behavior 159
 Contents • xi

5.3.2 Diet 163

5.3.3 Avoidance of arthropod vectors and parasites 165
5.3.4 Parental care 167
5.3.5 Avoiding infected conspecifics 168
5.4 Parasite pressure, mate choice, and sexual selection 170
5.4.1 Direct benefits: selection of uninfected caregivers 171
5.4.2 Avoidance of directly transmitted parasites 171
5.4.3 Indirect benefits of mate choice 172
5.4.4 Parasite status, resistance, and signals for choosing mates 173
5.5 Summary and synthesis 174

6 Infectious disease and primate social systems 176

6.1 Introduction 176

6.2 Variation in primate social systems 178
6.2.1 Chains of transmission within and among primate groups 182
6.3 Disease risk and primate social systems 184
6.3.1 Group size and contagious infections 184
6.3.2 Group size, flying insects, and vector-borne infections 187
6.3.3 Group composition 190
6.3.4 Group spread and contact within groups 190
6.3.5 Dispersal among groups 191
6.3.6 Territoriality and range overlap 192
6.4 Mating systems, sexual behavior, and STDs 193
6.4.1 Mating promiscuity 194
6.4.2 Effect of reproductive skew 195
6.4.3 Testing effects of STD risk on primate mating systems 195
6.5 Impacts of host behavior on pathogen evolution 197
6.5.1 Evolution of virulence 197
6.5.2 Evolution of transmission strategies 200
6.5.3 Coevolution 201
6.6 Methodological approaches to study effects of
parasites on host social systems 206
6.6.1 Fields studies 206
6.6.2 Directional tests using comparative methods 208
6.6.3 Incorporating parasites in comparative studies of sociality 209
6.6.4 Modelling approaches 209
6.7 Summary and synthesis 210

7 Parasites and primate conservation 213

7.1 Introduction 213

7.2 Parasites as a cause of wildlife declines 216
7.2.1 Emerging infectious diseases in primates and other wildlife 218
xii • Contents

7.3 Disease risk and anthropogenic change 227

7.3.1 Habitat destruction and degradation 227
7.3.2 Reductions in host population size 229
7.3.3 Human impacts on parasite biology 231
7.4 Conservation efforts in response to infectious disease risk 233
7.4.1 Monitoring parasites in wild populations 233
7.4.2 Reserve design and management 235
7.4.3 Captive breeding and semi-free-ranging populations 237
7.4.4 Ecotourism and scientific field research 240
7.4.5 Direct intervention to reduce the impact of disease 241
7.5 Evolutionary considerations and host–parasite biodiversity 244
7.6 Summary and synthesis 244

8 From nonhuman primates to human health

and evolution 248

8.1 Introduction 248

8.2 Origins and early history of infectious disease in humans 250
8.2.1 Infectious agents in early human societies 250
8.2.2 Epidemiological transitions and the rise of human pathogens 256
8.3 Human responses to infectious diseases: from Darwinian
medicine to public health 261
8.3.1 Behavioral responses to infectious diseases 264
8.3.2 Evolution of immune defenses and resistance traits 269
8.4 Global patterns of disease risk among contemporary human societies 272
8.5 Wild primates and emerging diseases in humans 276
8.6 Summary and synthesis 282

9 Concluding remarks and future directions 285

9.1 Introduction 285

9.2 What is the diversity of parasites in wild primates? 285
9.3 Population biology and impacts of parasites in wild primates 287
9.4 Immune and behavioral defenses: tradeoffs against different
infectious agents 289
9.5 What are the links between primate sociality and parasitism? 290
9.6 Are parasites a significant threat to primate conservation efforts? 292
9.7 From primates to understanding human-pathogen interaction 294
9.8 Concluding remarks 295

References 296

Index 369
1
Questions, terminology, and underlying
principles
1.1 Introduction
Parasites are ubiquitous in the lives of primates, and infectious diseases can cause
devastating mortality in wild populations, including recent deaths arising from Ebola
hemorrhagic fever and anthrax infections in African apes (Walsh et al. 2003b;
Leendertz 2004). An incredible diversity of parasites inhabits primate hosts,
including sexually transmitted viruses, insect-borne protozoa that cause malaria, and
helminths responsible for schistosomiasis and tapeworm infections. More than 50
different parasite species have been documented in some free-ranging primate
species, such as olive and yellow baboons (Nunn et al. 2003a), and an individual
primate may shed hundreds or thousands of parasite infectious stages over the course
of a single day (Pitchford and Visser 1975; Müller-Graf et al. 1996; Nizeyi et al.
1999).
Many of these infectious agents, such as simian immunodeficiency viruses (SIVs),
are relatively benign in their natural hosts, and thus have virtually undetectable effects
on primate fitness. Others, such as Ebola, have caused alarming declines in primate
populations and therefore play a major role in conservation efforts (Chapman et al.
2005a). Still other parasites, including intestinal worms and blood-borne protozoa,
have more cryptic effects on primate survival or fecundity in the short term, but taken
together their cumulative impacts could be enormous. Not to be overlooked are the
myriad of ways that parasites affect patterns of primate behavior, including foraging
decisions, behavioral defenses to insect vectors, and mating and social interactions.
Behavioral ecologists have highlighted a variety of ecological and social factors
that underlie primate mating and social systems, including predation, resource
competition, and inter-sexual conflict (Wrangham 1980; Dunbar 1988; van Schaik
1989, 1996; Smuts and Smuts 1993). Infectious disease represents another potential
ecological force in primate social evolution, but the role of parasites in primate
socioecology has received remarkably little attention compared to other factors. This
omission is extraordinary given that social animals such as primates are expected to
be at unusually high risk from infectious diseases, in part because greater contact
rates among individuals in social networks should facilitate the spread of infectious
disease (Møller et al. 1993; Altizer et al. 2003b). Primates are an ideal group for inves-
tigating the links between parasites and socioecology because much is known about
2 • Questions, terminology, and underlying principles

their basic biology, including life history traits, diet, habitat use, and mating patterns
(Smuts et al. 1987; Lee 1999; Kappeler and Pereira 2003). This extensive knowledge
base makes it possible to investigate the effects of parasites against the background
of other ecological forces that influence social systems.
The goal of this book is to examine the links between parasitism and primate
behavior, ecology and evolution. Although we focus on primates, many of the prin-
ciples and approaches developed here apply to a wide range of animals, including
other mammals, birds, and insects. A question central to this book is “what factors
influence disease risk”? In other words, what intrinsic host characteristics and
environmental parameters determine the number and types of parasites infecting
wild animals at the individual, population, and species levels? A second and related
question is “how can animals reduce this risk”? Data exist to test a broad range of
hypotheses related to these two questions, although further research is needed to
link many of these predictions with real-world data and to experimentally investi-
gate key hypotheses. Given recent theoretical and empirical developments in
wildlife epidemiology, this is an exciting and dynamic time to investigate these
questions. We cannot yet hope to provide a definitive treatise; instead, we identify
key hypotheses concerning the role of infectious disease in primate mating and
social systems, synthesize existing evidence for these hypotheses, and identify
future directions for testing predictions through field, comparative, and theoretical
approaches.
We also explore the implications of infectious disease in nonhuman primates for
both public health and conservation concerns. Humans are clearly the best studied
of all primate species in terms of infectious diseases, and pathogens continue to
impact human health around the world. The origins of multiple pathogens that
crossed into humans both recently and thousands of years ago can be traced to
nonhuman primates, with examples including malaria and several retroviral dis-
eases, the best known of which is HIV/AIDS. Understanding the links between
parasites and primate socioecology should provide new insights to human health
in a broad ecological and evolutionary context, expanding the domain of
Darwinian medicine (Ewald 1980; Nesse and Williams 1996; Stearns 1999;
Trevathan et al. 1999), and generating new hypotheses to test across human
societies at a global scale (Low 1987; Guegan et al. 2001; Guernier et al. 2004).
Furthermore, epidemiological insights drawn from studies of infectious diseases in
humans can advance our understanding of disease spread in nonhuman primates,
which is critical for conserving endangered primates increasingly at risk from
emerging pathogens and other anthropogenic threats (Wallis and Lee 1999;
Walsh et al. 2003b).
To set the stage for the rest of the book, in this introductory chapter we begin by
defining key terms and providing a historical overview of previous research on the
interplay between ecological factors and primate sociality. To emphasize the
ecological impacts of infectious diseases and their potential role as selective agents,
we conclude the chapter by reviewing the effects of parasites on host fitness in wild
primate populations.
 Essential terminology: parasite, disease, and disease risk • 3

1.2 Essential terminology: parasite, disease,

and disease risk
1.2.1 What is a parasite?
The word parasite has different meanings depending on the discipline in which it is
used and how it is applied. In this book, we use the ecological definition of a parasite
as any organism that lives on and draws nutrients from another living organism (the
host), usually to the host’s detriment. Parasites not only drain material resources
from their hosts, but can also exploit host metabolism and behavior. Combes (2001)
refers to host–parasite relationships as “durable interactions”, in contrast to predator–
prey relationships that are of shorter duration and result in death of the prey. The
definition of parasite we use excludes some groups of organisms that have a close
association with primate hosts, such as symbiotic bacteria that aid digestion of leaves
in colobines (Bauchop and Martucci 1968). This definition also excludes mosquitoes
and other highly mobile arthropods that feed on blood or other host resources. As
with predators, their associations with hosts tend to be ephemeral at the level of
individual animals; hence, these biting insects are more accurately described as
“micro-predators” (Bush et al. 2001). However, many blood-feeding arthropods play
an important role as vectors for parasites that infect primate hosts, including
vector-borne protozoa, nematodes, and viruses. As such, many behavioral defenses
against parasitism target arthropod vectors that are responsible for the spread of
these parasites.
An important distinction made by Anderson and May (1979, 1991) is that
parasitic organisms can be categorized either as microparasites or as macroparasites.
Microparasites are often referred to as pathogens or disease-causing microbes and
include viruses, bacteria, protozoa, and fungi, whereas macroparasites typically
include worms (helminths) and arthropods. The distinction between micro- and
macroparasites is useful to ecologists and epidemiologists, as these groups differ in
the degree of within-host replication, factors affecting their population dynamics,
and how they are measured in natural populations. Later chapters address these
fundamental differences in more detail, and also consider additional classifications
of parasites, with special attention to parasite characteristics that govern their trans-
mission within populations and between species.

1.2.2 Parasite and disease

The terms “parasite” and “disease” are often used interchangeably, yet it is incorrect
to do so. Disease refers to the pathology caused by infection, including outward
physical signs and internal or behavioral changes, whereas parasites are the disease-
causing organisms. A related term is pathogen, which refers to any disease-causing
agent, although this term is most commonly used for microbial parasites (viruses and
bacteria). In this book, we primarily use the term parasite to refer to all infectious
4 • Questions, terminology, and underlying principles

organisms that can potentially harm their hosts, but occasionally substitute related
words when appropriate (e.g. pathogen, infectious agent).
Although not all infections are pathogenic, parasitic organisms can cause a stag-
gering array of pathologies in primate hosts (e.g. Kuntz 1982). These manifestations
might result directly from activities of the parasite, as in the painful migration of war-
ble flies through the flesh of large mammals (Bush et al. 2001; Colwell 2001), or as
diarrhea resulting from reduced intestinal water absorption caused by Giardia (Olson
and Buret 2001). Physiological consequences of parasite infection in the host usually
fall into one of three categories—those that benefit the parasite, those that benefit the
host, and those that are byproducts of infection and benefit neither host nor parasite
(Ewald 1980; Dawkins 1982; Holmes and Zohar 1994; Thompson 1994b). For exam-
ple, several arthropod-borne parasites clog the insect vector’s digestive systems and
impair their ability to obtain a full blood meal, thereby increasing the biting rate of
these vectors to the parasites’ advantage (and to the detriment of the host, Koella et al.
1998). On the other hand, a rise in host body temperature (fever) following infection
can interfere with the growth of some parasites and facilitate a more intense immune
response, in this case to the host’s advantage (Ewald 1994a).
In some situations, pathology produced by the host’s body in the context of
infection actually can be harmful to host survival and reproductive success. Consider,
for example, the famous images of elephantiasis of the lower extremities (lymphatic
filariasis; Fig. 1.1). These horrifying pathologies are the result of complex, long-term
immune responses to the mosquito-transmitted nematodes Brugia malayi and
Wuchereria bancrofti (Bush et al. 2001). Interestingly, B. malayi is documented to
occur in free-living Southeast Asian monkeys (Laing et al. 1960; Mak et al. 1982),
but in these species the parasite does not cause the striking pathology found in
humans (Orihel and Seibold 1972).
Parasites that induce detrimental pathology in hosts are more likely to regulate
populations than those with weaker effects on host fitness (Scott and Dobson 1989).
But it is important to keep two caveats in mind. First, when parasites affect host
survival alone, standard host–parasite models (Anderson and May 1979, 1991)
predict that parasites with low or intermediate effects on hosts will depress host
density to a greater extent than parasites that cause high host mortality. This occurs
because extremely harmful parasites are likely to kill their hosts before new trans-
mission events occur, highlighting the kinds of insights that emerge when questions
are addressed from a rigorous epidemiological modeling perspective—an approach
described in later chapters. Thus, an important point to emerge from models is that
parasites with low or moderate effects on hosts should not be overlooked when assess-
ing sources of disease risk and potential causes of wildlife declines (McCallum
1994; McCallum and Dobson 1995). This point especially applies to parasites that
affect host fecundity (or, in extreme cases sterilize their hosts), as theory predicts
that such parasites can limit host recruitment and cause extreme reductions in host
population size.
Second, counter to conventional wisdom, the most frequently observed parasites
are not necessarily the ones most responsible for population declines (Anderson
 Essential terminology: parasite, disease, and disease risk • 5

Fig. 1.1 Woman in Ghana exhibits elephantiasis of the right leg and oedema of the left leg.
Reprinted from the World Health Organization (WHO/TDR/Crump, image 9902944).

and Gordon 1982). Mathematical models predict that highly transmissible micro- or
macroparasites with little or no fitness effects should be relatively common at the
population level. In this case, the general host population will show relatively high
levels of infection, and the parasite will be found incidentally among a large number
of animals that die. Thus, high rates of parasitism in morbid or dead hosts do not
necessarily indicate that the parasite in question is having a major impact on the pop-
ulation (McCallum and Dobson 1995). Later in this chapter and subsequent chap-
ters, we discuss more appropriate ways to measure population-level impacts of
parasites (Gulland 1992; Hudson et al. 1998b).

1.2.3 What is disease risk and how is it measured?

Throughout this book we refer to “disease risk” as the probability of acquiring an
infectious disease. In using this term, we are approaching questions from the host’s
perspective, as the parasite would view this as an opportunity rather than a risk.
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