How do infectious diseases spread through host populations, and under what conditions will parasites regulate host abundance? What features of host and parasite biology determine the probability of parasite invasion and persistence? As illustrated in Chapter 3, ecologists can explore factors associated with disease risk using descriptive data on host biology and parasite occurrence. Indeed, primates provide many fascinating examples of how host biology and environmental variables can influence variation in parasite occurrence. To move beyond qualitative and largely intuitive approaches, more quantitative methods can be used for investigating host-parasite dynamics. Such approaches are especially important for real-world systems where multiple ecological, behavioral, and genetic processes interact.

Much of our understanding of wildlife-pathogen systems has been shaped by mathematical models that examine how events that occur at the level of individual animals—including birth, infection, dispersal, and death—translate into populationlevel phenomena such as epidemic cycles or the spread of infectious diseases across a geographic region. From a practical perspective, conclusions arising from even the simplest of models can help assess the probability of parasite invasion and develop control strategies for mitigating these risks in wild populations. These approaches are also important for zoo collections or breeding facilities, where the introduction of one infected animal (or the transfer of diseases among species) can devastate an entire captive population. In a public health context, mathematical models have been applied to develop strategies for containing threats arising from pathogens like SARS, HIV/AIDS, and potential bioterror agents in human populations (Anderson et al. 1989; Halloran et al. 2002; Lipsitch et al. 2003; Smith and Blower 2004). Similar approaches can be used to predict and manage the spread of infectious diseases in primate species, given sufficient information on host and parasite characteristics and collaboration between theoreticians, wildlife veterinarians, and field primatologists (Stuart and Strier 1995; Heymann 1999).

4.1.1 An historical perspective

Traditionally, epidemiology refers to the study of disease processes in humans, but increasingly this term has been applied to nonhuman systems as well. The related term epidemic—translated literally as "to come upon people"—defines a rapid increase in the prevalence or intensity of parasitic infection beyond what is normally present. This is in contrast to the term endemic, used to describe infections that are established and constantly present in a particular region and normally do not show large fluctuations in occurrence or area affected.

Many historians recognize the origins of epidemiology in the early ground-breaking work of Dr John Snow, who in 1854 used data from the location of cholera deaths to identify the Broad Street pump as the source of a cholera outbreak in London (Rosenberg 1962; CDC 2004a). Dr Snow reportedly had this pump handle removed and the outbreak subsided. His work led to the development of a new theory that cholera was transmitted primarily through contaminated water, and thus pointed the way toward public health reforms to limit disease spread, including improved sanitation (CDC 2004a). In terms of understanding the dynamics of human diseases, other groundbreaking work during this past century emerged from long-term studies of measles and other communicable childhood diseases (Soper 1929; Bartlett 1957, 1960). The dynamics of measles in European cities probably represents one of the most comprehensively studied data sets in ecology, and analyses of monthly case reports of this viral infection have tremendously advanced knowledge of host-pathogen interactions (Bj0rnstad et al. 2002; Grenfell 2002). For example, Bartlett's (1957, 1960) seminal work on the epidemics of measles in English and Welsh towns before the advent of vaccination gave rise to the concept of a "critical community size," namely the minimum population size above which an infection persists in the population.

Parasitologists and veterinary workers studying infectious diseases in animals have contributed extensively to descriptions of parasite taxonomy, life cycles, pathology, and pathogen occurrence. This work uncovered important details of parasite biology from a variety of wild animals, including nonhuman primates (Fiennes 1967; Fowler 1976; Kalter 1983; Brack 1987). Also of historical note are detailed studies of gastrointestinal helminths during the last century that pointed to the role of temperature and moisture in determining parasite outbreaks in sheep and cattle (Gordon et al. 1934; Levine 1963), and more generally set the stage for later studies of the links between climate and the ecology of infectious diseases (Dobson and Carper 1992; Harvell et al. 2002). By focusing on the life history of parasites or infections within single animals, however more traditional approaches in parasitol-ogy overlooked many important ecological processes, including the role of parasites in regulating animal abundance, factors determining the spread of parasites through populations, and the potential for evolutionary change in both hosts and parasites (Anderson 1995; Tompkins et al. 2001; Hudson et al. 2002; Altizer et al. 2003a).

Beginning in the late 1970s, a synthetic view of the ecological dynamics of host-parasite interactions was initiated by a series of ground-breaking papers by Roy Anderson and Robert May (Anderson and May 1979; May and Anderson 1979). Their work joined fundamental approaches in population ecology with the biological details of host-parasite interactions using epidemiological frameworks dating back to the first part of the twentieth century (Ross 1911; Kermack and McKendrick 1927). Anderson and May's models showed that parasite establishment in host populations is linked fundamentally to host abundance and behavior (Anderson and May 1978). These models further revealed the ways that parasites can regulate populations and identified mechanisms that limit the spread of parasites (May and Anderson 1978). A combination of modeling work and epidemiological data provided new perspectives on the dynamics of infectious diseases in humans (Anderson and May 1991; Earn et al. 2000; Grassly et al. 2005), and these general principles have been applied across a wide range of host-parasite systems. Indeed, studies of infectious disease dynamics surged during the 1980s and 1990s, and scientific investigation in this field continues to expand to this day (Figure 4.1), as evidenced by a large number of scientific books and edited volumes addressing host-parasite ecology and evolution published in the last decade (Grenfell and Dobson 1995; Clayton and Moore 1997; Frank 2002; Hudson et al. 2002; Moore 2002; Thomas et al. 2004a).

Recent progress in the field of wildlife disease ecology has emerged from efforts to apply experimental and modeling approaches to parasite spread and population dynamics in natural populations (Grenfell and Dobson 1995; Hudson et al. 2002),

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