Summary and synthesis

A general understanding of parasite ecology and epidemiology is essential for managing infectious diseases in nonhuman primates and other wild animal populations, both in terms of detecting disease threats for vulnerable species and implementing control measures to decrease pathogen pressure. Basic epidemiological models give rise to several key principles that characterize host-parasite interactions. These include the concept of the basic reproductive number, R0, which sets the criteria for parasites to establish in a population and also provides information on how rapidly pathogens will spread in a naive population. Mathematical models point to situations in which parasites will regulate or reduce the size of host populations and show when social and spatial heterogeneities are likely to be important in wildlife-pathogen systems.

Among wild primates, a large number of field studies have examined patterns of habitat use, demography, and social interactions. We also know that primates harbor an incredible diversity of parasites and infectious diseases (Chapman et al. 2005a; Nunn and Altizer 2005). Yet surprisingly few studies have linked host characteristics, including abundance, life history traits, and behavior with patterns of parasite occurrence. Furthermore, no comprehensive experimental studies addressing parasite ecology have been conducted in wild primate populations (even though such experiments are feasible, Janson 2000). Inferences of the population impacts of primate parasites are therefore made indirectly, except where conspicuous epidemics have decimated previously intact primate populations (Chapter 1). One priority for the future is to collect comprehensive monitoring data for a variety of disease-causing agents in wild primates (Chapter 7), including those shared with human hosts (Chapter 8, Wolfe et al. 1998).

For species of conservation concern like many primates, non-invasive sampling techniques should prove to be extremely useful for monitoring the occurrence of infectious diseases (Makuwa et al. 2003). One promising example is the use of fecal samples for epidemiological studies of a range of gut-dwelling parasites. More recent molecular techniques have proven useful for extracting DNA or RNA of viral pathogens from fecal material, including agents not typically associated with gut infections, such as SIV infections in wild chimpanzees and sooty mangabeys (Ling et al. 2004; Nerrienet et al. 2005). The advantage is that researchers could determine the hosts' infection status, and by amplifying portions of the parasite's genome, could also obtain molecular data useful for investigating the epidemiology of parasite populations. Studies of feces could be further used for assessing the magnitude and timing of host responses by detecting the presence of host mucosal antibodies to particular pathogens, and by measuring levels of stress hormones, such as corticosterone, present in fecal material. Host genetic data has been obtained from non-invasive samples such as hair and feces in several primate species, including baboons, Barbary macaques, chimpanzees, and gorillas (Smith et al. 2000; Jensen-Seamann and Kidd 2001; Lathuilliere et al. 2001; Morin et al. 2001; Lukas et al. 2004). Combining host genetic data with monitoring of parasites in wild primate populations could potentially point to factors that underlie primate susceptibility to infectious diseases, and would allow biologists to explore the consequences of disease for shifts in the genetic composition and long-term viability of primate populations (Altizer et al. 2003a).

The shortage of detailed studies of primate-parasites dynamics calls for better integration of quantitative theoretical approaches and records of parasitism in natural populations. For example, it is difficult to relate categorically defined mating systems (e.g. polygyny, serial monogamy) and social organization (e.g. solitary, fission-fusion communities) to the spread of parasites in wild populations. More precise measures of parameters suggested by theoretical models are needed from wild mammal populations, including inter- and intra-group contact rates, dispersal rates and distances, contact durations for different types of social interactions, and better measures of variance in male and female mating success. Moreover, model parameters that define contacts leading to parasite transmission must reflect biologically realistic and estimable processes, which can be achieved by increasing interactions between primatologists and epidemiologists. Indeed, perhaps the greatest challenge in moving forward studies of parasite-pathogen interactions is to increase communication and collaboration between mathematical ecologists studying the dynamics of infectious diseases, veterinary workers collecting samples from the field, and behavioral ecologists collecting detailed records of primates in their natural environments.

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