Infectious Diseases in Primates Behavior,

Recent progress in the field of wildlife disease ecology demonstrates thatinfectious disease plays a crucial role in the lives of wild animals. Parasitesand pathogens should be especially important for social animals in which highcontact among individuals increases the potential for disease spread. As one ofthe best studied mammalian groups, primates offer a unique opportunity toexamine how complex behaviours (including social organization) influence therisk of acquiring infectious diseases, and the defences used by animals to avoidinfection. This book explores the correlates of disease risk in primates,including not only social and mating behaviour but also diet, habitat use, lifehistory, geography and phylogeny. The authors examine how a core set of host andparasite traits influence patterns of parasitism at three levels of biologicalorganization: among individuals, among populations, and across species.A major goal is to synthesize, for the first time, four disparate areas ofresearch: primate behavioural ecology, parasite biology, wildlife epidemiology,and the behavioural and immune defences employed by animals to counterinfectious disease. Throughout, the authors provide an overview of theremarkable diversity of infectious agents found in wild primate populations.Additional chapters consider how knowledge of infectious diseases in wildprimates can inform efforts focused on primate conservation and human health.More generally, this book identifies infectious disease as an important frontierin our understanding of primate behaviour and ecology. It highlights futurechallenges for testing the links between host and parasite traits, includinghypotheses for the effects of disease on primate social and mating systems.

Charles Nunn is a research scientist at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany and an Assistant Professor in the Department of Integrative Biology at the University of California in Berkeley, USA. His research interests include primate behaviour, disease ecology and comparative biology.
Sonia Altizer is an Assistant Professor at the Institute of Ecology of the University of Georgia. Her research focuses on the ecology and evolution of host-pathogen interactions in wild animal populations.

Questions, terminology, and underlying principles	p. 1
Introduction	p. 1
Essential terminology: parasite, disease, and disease risk	p. 3
What is a parasite?	p. 3
Parasite and disease	p. 3
What is disease risk and how is it measured?	p. 5
Ecological drivers of primate sociality	p. 8
Between-group resource competition	p. 9
Predation and within-group competition	p. 9
Inter-sexual conflict	p. 10
Infectious disease	p. 10
Fitness consequences of parasites in wild primate populations	p. 14
Organizational layout of this book	p. 20
Diversity and characteristics of primate parasites	p. 22
Introduction	p. 22
Taxonomic diversity of parasites from wild primates	p. 26
Viruses	p. 29
Bacteria	p. 33
Fungi	p. 34
Protozoa	p. 35
Helminths	p. 37
Arthropods	p. 40
Strategies for parasite transmission	p. 42
Host specificity and "multi-host" parasites	p. 45
Virulence: negative effects of parasites on their hosts	p. 48
Parasite transmission and manipulation of host behavior	p. 52
Causes and consequences of altered behavior	p. 54
Manipulation of primate hosts	p. 54
Summary and synthesis	p. 55
Primate socioecology and disease risk: predictions and rationale	p. 57
Introduction	p. 57
Background concepts	p. 61
Encounter and infection probability	p. 61
Formulating hypotheses at individual and comparative levels	p. 64
Host traits and disease risk	p. 65
Body mass, life history, and individual age	p. 65
Host population size and density	p. 71
Social organization, group size, and dominance rank	p. 74
Reproduction, mating behavior, and sex differences	p. 80
Ranging behavior, substrate use, and diet	p. 86
Environmental factors and seasonality	p. 92
Summary and synthesis	p. 95
Host-parasite dynamics and epidemiological principles	p. 98
Introduction	p. 98
An historical perspective	p. 98
Basic terminology and measures of infection	p. 101
Analytical models of disease spread	p. 103
Microparasites and compartment models	p. 106
Macroparasite models	p. 115
The role of parasites in regulating host populations	p. 117
Theoretical predictions	p. 117
Regulation in experimental and natural populations	p. 119
Heterogeneities and dynamical complexities	p. 122
Spatial heterogeneity: landscape features and metapopulation dynamics	p. 122
Host social system	p. 123
Multi-host dynamics	p. 128
Summary and synthesis	p. 132
Host defenses: the immune system and behavioral counterstrategies	p. 134
Introduction	p. 134
Responding to infections: strategies for parasite removal	p. 135
Immune defenses	p. 135
Physiological responses and sickness behaviors	p. 148
Grooming as a means of parasite removal	p. 150
Medicinal plant use	p. 155
Preventing infections: strategies for parasite avoidance	p. 159
Habitat use and ranging behavior	p. 159
Diet	p. 163
Avoidance of arthropod vectors and parasites	p. 165
Parental care	p. 167
Avoiding infected conspecifics	p. 168
Parasite pressure, mate choice, and sexual selection	p. 170
Direct benefits: selection of uninfected caregivers	p. 171
Avoidance of directly transmitted parasites	p. 171
Indirect benefits of mate choice	p. 172
Parasite status, resistance, and signals for choosing mates	p. 173
Summary and synthesis	p. 174
Infectious disease and primate social systems	p. 176
Introduction	p. 176
Variation in primate social systems	p. 178
Chains of transmission within and among primate groups	p. 182
Disease risk and primate social systems	p. 184
Group size and contagious infections	p. 184
Group size, flying insects, and vector-borne infections	p. 187
Group composition	p. 190
Group spread and contact within groups	p. 190
Dispersal among groups	p. 191
Territoriality and range overlap	p. 192
Mating systems, sexual behavior, and STDs	p. 193
Mating promiscuity	p. 194
Effect of reproductive skew	p. 195
Testing effects of STD risk on primate mating systems	p. 195
Impacts of host behavior on pathogen evolution	p. 197
Evolution of virulence	p. 197
Evolution of transmission strategies	p. 200
Coevolution	p. 201
Methodological approaches to study effects of parasites on host social systems	p. 206
Fields studies	p. 206
Directional tests using comparative methods	p. 208
Incorporating parasites in comparative studies of sociality	p. 209
Modelling approaches	p. 209
Summary and synthesis	p. 210
Parasites and primate conservation	p. 213
Introduction	p. 213
Parasites as a cause of wildlife declines	p. 216
Emerging infectious diseases in primates and other wildlife	p. 218
Disease risk and anthropogenic change	p. 227
Habitat destruction and degradation	p. 227
Reductions in host population size	p. 229
Human impacts on parasite biology	p. 231
Conservation efforts in response to infectious disease risk	p. 233
Monitoring parasites in wild populations	p. 233
Reserve design and management	p. 235
Captive breeding and semi-free-ranging populations	p. 237
Ecotourism and scientific field research	p. 240
Direct intervention to reduce the impact of disease	p. 241
Evolutionary considerations and host-parasite biodiversity	p. 244
Summary and synthesis	p. 244
From nonhuman primates to human health and evolution	p. 248
Introduction	p. 248
Origins and early history of infectious disease in humans	p. 250
Infectious agents in early human societies	p. 250
Epidemiological transitions and the rise of human pathogens	p. 256
Human responses to infectious diseases: from Darwinian medicine to public health	p. 261
Behavioral responses to infectious diseases	p. 264
Evolution of immune defenses and resistance traits	p. 269
Global patterns of disease risk among contemporary human societies	p. 272
Wild primates and emerging diseases in humans	p. 276
Summary and synthesis	p. 282
Concluding remarks and future directions	p. 285
Introduction	p. 285
What is the diversity of parasites in wild primates?	p. 285
Population biology and impacts of parasites in wild primates	p. 287
Immune and behavioral defenses: tradeoffs against different infectious agents	p. 289
What are the links between primate sociality and parasitism?	p. 290
Are parasites a significant threat to primate conservation efforts?	p. 292
From primates to understanding human-pathogen interaction	p. 294
Concluding remarks	p. 295
References	p. 296
Index	p. 369
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Infectious Diseases in Primates Behavior, Ecology and Evolution

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