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Female lambs

Female yearlings

Male yearlings

Fig. 1.5 Mortality of Soay Sheep on the Island of St. Kilda following a population crash that occurred in 1992. Dark bars show sheep that were treated orally with an antihelminthic drug several months prior to the crash, and light bars show control (untreated) sheep. Sample sizes are shown above each bar. Reprinted from F. M. D. Gullard, S. D. Albon, et al., "Parasite associated polymorphism in a cyclic ungulate population," Proceedings of the Royal Society Series B, vol. 254, 7-13. Copyright (1993) by the Royal Society.

(O'Lorcain and Holland 2000). Subtle effects of parasitism, such as reduced cognition, memory loss, or learning impairment, might be among the most difficult to quantify in the wild, but should be exceptionally important in free-living animals such as primates that rely heavily on cognitive skills. For example, it would be fascinating to compare the foraging success of parasitized and un-parasitized spider monkeys that must remember the location of dispersed fruiting trees.

In summary, abundant evidence points to the existence of parasite-induced reductions in host fitness among free-living primates. These cumulative studies are important not only from the perspective of host regulation or parasite-mediated population declines, but also because they reveal that parasites can act as powerful selective agents in natural populations. Thus, host species exposed to a diverse array of parasites are expected to evolve behavioral, innate, or inducible defenses to resist or reduce the impacts of parasites and pathogens (Nunn et al. 2000; M0ller et al. 2001). This prediction hinges upon demonstrating costs of infection for host survival and fecundity (in other words, demonstrating that parasites impose selection gradients at the population level). In fact, if group living and social contacts increase exposure to a variety of parasites, then highly social species should be under the greatest pressure to invest resources into anti-parasite counterstrategies. This is one of the major unexplored frontiers of studies in primate socioecology, offering great opportunities for researchers, while also providing new insights to human evolution and primate conservation.

1.5 Organizational layout of this book

This book is organized into eight chapters, moving from essential background material to a synthetic framework, and finally to applied examples in primate conservation and human health. Chapter 2 reviews the biological features of major groups of parasites and links these features to specific aspects of disease risk in primates. Chapter 2 therefore identifies parasite characteristics that are most important to understanding patterns of disease risk, including transmission strategy, host specificity, parasite life cycles, virulence, and how parasites manipulate host behavior to enhance their transmission.

Chapter 3 discusses the underlying rationale for factors that influence disease risk in primates at two levels: among individuals and across species. Throughout Chapter 3, we summarize primate behavioral and ecological traits that are essential for understanding disease risk, including dominance rank, group size and composition, dispersal, mating system, and ecological factors that correlate with these social system parameters, such as body mass, life history characters, and use of the ground versus trees for locomotion (substrate use).

Chapter 4 links host and parasite ecology by considering basic epidemiological parameters and processes, and it covers how disease patterns scale up from individuals to populations and communities. We discuss factors affecting the transmission dynamics of parasites, including the basic reproductive number R0, the aggregation of macroparasites within populations, and frequency- versus density-dependent transmission. This chapter also considers how parasites might regulate primate populations or influence host abundance through their effects on survival and fecundity.

Chapter 5 focuses on the host's response to parasitism by considering behavioral and immunological defenses to infectious disease. In this chapter, we concentrate on the individual level by considering how primate immune systems defend against parasite infections, how animals use medicinal plants, and the avoidance of sick individuals. We also investigate the links between sexual selection and parasitism in primates, focusing in particular on mate choice.

Chapter 6 is a synthetic chapter that integrates material from the previous chapters to explore the ways in which parasites might influence primate mating and social systems. We consider how individual responses to parasitism can influence social system characteristics, and we raise the question of causality, namely, "do host traits influence patterns of parasitism, or do parasites influence patterns of sociality?" These are not mutually exclusive questions, but by considering a coevolutionary model of host and parasite traits, we can begin to address the multiple ways in which lineages of hosts and parasites interact.

Chapters 7 and 8 extend the basic framework developed in earlier chapters to applied questions in primate conservation and human health. In Chapter 7, we examine the conservation implications of parasites, including cross-species transmission, the effects of eco-tourism, and approaches to control epidemics in wildlife. We also consider the potential longer-term benefits of maintaining intact communities of hosts and parasites. In Chapter 8, we consider how understanding infectious disease in nonhuman primates provides insights to human health. In particular, we examine the origins of human infectious diseases and their impacts in a historical context. More speculatively, we ask how behavioral counterstrategies to infectious disease in nonhuman primates pertain to understanding human behavior in the context of Darwinian medicine (Ewald 1980; Nesse and Williams 1996; Stearns 1999; Trevathan et al. 1999). We also discuss the role of wild primates in the maintenance of zoonotic pathogen and disease emergence, and we apply the concept of disease risk to investigate variation in human infections at global and regional scales.

Throughout this book, we aim to synthesize existing knowledge in ways that will lead to new questions, thus pointing the way toward future research on infectious disease and behavioral ecology in primate hosts and other animals. This goal is achieved through a "summary and synthesis" at the end of individual chapters, and with a final chapter (Chapter 9) that reviews key points in the book and identifies major questions for future research.

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