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All subadults in these populations probably were low ranking, potentially confounding the effect of age with that of dominance rank.

Other studies found no significant effect of age on disease risk, or even patterns opposite to predictions. For example, Sanchez-Villagra et al. (1998) found no age-related differences in ectoparasite loads in red howler monkeys, and a study of mantled howlers found no differences among age classes in infection with intestinal helminths (Stuart et al. 1998). Among baboons, younger animals showed greater prevalence and intensity of infection with both endoparasitic worms and ectoparasites. Thus, Eley et al. (1989) reported that juvenile baboons exhibited greater infestation with lice nits (eggs). For five classes of helminths analyzed in olive baboon feces at Gombe, only one parasite showed an association with age, with prevalence and intensity of the nematode Strongyloides found to be significantly higher in younger animals (Müller-Graf et al. 1996). In another study, the prevalence of Schistosoma mansoni was again higher in younger baboons, with results approaching significance (p = 0.051, Müller-Graf et al. 1997). The authors suggested that this pattern was probably caused by differences in encounters with parasites, as younger baboons contact water more frequently than adults. Meade (1984) found that rates of infection with Strongyloides were highest in baboon and vervet infants, possibly because this nematode is transmitted vertically to infants from their mothers, and partial immunity then develops and persists into adulthood.

Fewer comparative studies have examined associations between parasitism and life history traits across species of primates or other mammals. Among anthropoid primates, Nunn et al. (2003a) found a positive effect of host longevity (measured as maximum life expectancy) on the diversity of protozoan parasites, but these results were driven by several outliers. Arneberg (2002) found no effect of longevity in his study of 45 species of mammals. In a comparative study of 23 mammals, however, Morand and Harvey (2000) found a negative association between longevity and helminth species richness after controlling for basal metabolic rate, body mass, and sampling effort, suggesting that parasites could be an important factor that reduces host longevity.

3.3.2 Host population size and density

Jared Diamond, in his (1997) book Guns, Germs and Steel, highlighted three factors that "launched the crowd of infectious diseases" in human populations. These included a more sedentary lifestyle (resulting from agriculture), increased world trade, and perhaps most importantly, the growth of urban centers associated with densely packed human populations (see also McNeill 1977; Anderson and May 1991). Indeed, a large number of epidemiological models, supported by data from several empirical studies, point to strong links between host density or population size and the spread of directly transmitted parasites, not just in humans, but across a wide array of host species (Chapter 4 and Anderson and May 1979; Arneberg 2002; Swinton et al. 2002). A broad range of mathematical models suggest that total host abundance is probably the major factor affecting transmission between host individuals for many parasite species (Anderson and May 1991). Total host abundance in this case refers to population size over an area where uniform contacts are likely to occur, and a key assumption in these models is that host populations are well-mixed, meaning that all individuals have an equal probability of contacting other individuals in the population—an assumption that is addressed in Chapter 4.

Hosts living at high density or with large populations and frequent intraspecific contacts should accumulate more parasite species (reviewed in Morand 2000; Roberts et al. 2002; Poulin and Morand 2004), but the predicted positive relationship between host abundance and pathogen fitness is subject to two caveats. First, this relationship probably applies best to directly-transmitted contagious parasites for which host contact rates increase with population size or density (Getz and Pickering 1983), and will be less important for vector-borne parasites and STDs where transmission is decoupled from host population density (Thrall et al. 1993a, 1998; Thrall and Antonovics 1997). An additional complicating factor involves identifying the natural unit or spatial scale at which population density or abundance affects disease transmission (Swinton et al. 2002). Thus, metapopulation models have shown that certain pathogens can persist even in low density host populations, provided that spatial heterogeneities and host dispersal generates sufficient opportunities for disease transmission (Hess 1996; Keeling 1999b).

3.3.2.1 Evidence for effects of population density or size

Few studies of disease risk within species of wild primates have examined the role of host population size directly. In a comparison of muriquis (Brachyteles arachnoides) in different habitats, Stuart et al. (1993) found that animals from the largest population exhibited the highest prevalence and species richness of intestinal parasites. The authors described their result as "unexpected" because this population also exhibited the lowest local density. However, this observed pattern highlights the importance of understanding the spatial scale at which host contacts and parasite transmission occur. In this case, total population size might have affected parasite establishment more so than local density. Other explanations are also possible, including the use of medicinal plants in the population with fewer parasites (Strier 1992, 1993).

Empirical studies of mammals have investigated the importance of local population density in explaining patterns of parasitism through time (Dobson and Meagher 1996b), across populations (Stuart et al. 1990; Stoner 1996), and across species (Arneberg et al. 1998). Several studies of primates attributed differences in levels of infection to variation in host population density. For example, Chapman et al. (2005a) found that prevalence of Trichuris increased with increasing host density in two species of colobines during population changes associated with logging. Similarly, Stuart et al. (1990) found higher prevalence of intestinal parasites in mantled howler monkeys at La Pacifica relative to less dense populations in Santa Rosa (both sites are in Costa Rica). On the other hand, a later study (Stoner 1996) compared prevalence at La Pacifica with a population of mantled howlers at La Selva,

Costa Rica, and found that prevalence was higher in the low-density population, with 100% of the individuals at La Selva harboring two or more parasite species based on fecal samples. These conclusions must be interpreted cautiously because comparison of only two populations makes it difficult to rule out the effects of other variables (e.g. McGrew et al. 1989a; Garland and Adolph 1994; Stuart and Strier 1995). For example, at La Selva, howler monkey populations probably experienced a moister environment, and other habitat variables might have contributed to differences between these populations (see Stoner 1996).

A comparative study also tested the importance of population density in explaining patterns of parasite species richness in anthropoid primates. In this study, Nunn et al. (2003a) controlled for other factors, including host life history, diet, and geographic range size. Population density emerged as the most consistent host trait that influenced overall parasite diversity (Fig. 3.7). Density also correlated positively with the diversity of viruses, protozoa, and helminths tested separately. In subsequent analyses, significant results were obtained when using an estimate of population size, measured as density multiplied by geographic range size. Studies by Arneberg and colleagues found similar relationships between population density and the diversity of helminths across a wider range of mammals (Arneberg et al. 1998, 2002).

Residual host population density

Fig. 3.7 Relationship between population density and overall parasite species richness in primates. Plots show the relationship between host population density (after controlling for body mass by taking residuals) and the size of the parasite community (after controlling for sampling effort by taking residuals). Similar results were obtained when sampling effort was controlled in three ways, with results here shown using Web of Science citation counts. Data points represent independent contrasts (as described in Box 3.2). From Nunn et al. 2003: Comparative tests of parasite species richness in primates. American Naturalist 162:597-614. Copyright 2003 by The University of Chicago Press.

Residual host population density

Fig. 3.7 Relationship between population density and overall parasite species richness in primates. Plots show the relationship between host population density (after controlling for body mass by taking residuals) and the size of the parasite community (after controlling for sampling effort by taking residuals). Similar results were obtained when sampling effort was controlled in three ways, with results here shown using Web of Science citation counts. Data points represent independent contrasts (as described in Box 3.2). From Nunn et al. 2003: Comparative tests of parasite species richness in primates. American Naturalist 162:597-614. Copyright 2003 by The University of Chicago Press.

In their study of 23 non-primate mammals, however, Morand and Harvey (2000) found no effect of density on helminth species richness. Another study investigated the relative effects of population size and density in fish and found that total population size, but not density, explained species richness and abundance of directly transmitted parasites (Bagge et al. 2004). Future comparative research could investigate patterns among parasites grouped by transmission strategy, focusing especially on directly transmitted parasites, and could also use independently derived estimates of total population size to better assess the independent effects of density, geographic range size and overall population size on levels of parasitism.

3.3.3 Social organization, group size, and dominance rank

Social interactions form the network of contacts through which many parasites spread (Anderson and May 1979, 1991). If close proximity or contact among host individuals increases parasite transmission, then greater degrees of host sociality or gregariousness should translate to higher parasite prevalence, intensity, and diversity (M0ller et al. 1993; Altizer et al. 2003b). Highly social host species are therefore predicted to suffer greater exposure to parasites (Brown and Brown 1986; M0ller et al. 2001), experience increased selection for immune defenses, and evolve behavioral defenses against parasites (Chapter 5, 6, and Freeland 1979; Loehle 1995). Population density is the key socioecological variable incorporated into standard epidemiological models (Chapter 4 and Anderson and May 1979), but group size is a major component of social organization that is widely viewed as increasing disease risk in primates (Freeland 1976; Davies et al. 1991; Tutin 2000) and other animals (see M0ller et al. 1993; Cote and Poulin 1995; Krause and Ruxton 2002). More recently, however, it has been proposed that by subdividing populations into smaller groups, social organization could actually reduce disease risk. We examine these alternative scenarios and then review empirical evidence for effects of group size on disease risk in primates.

Several processes indicate that group size should increase with the risk of infection by directly transmitted parasites. First, group size represents a measure of local population density, specifically the density of hosts in their typical social environments. Second, the number of contacts among hosts may be greater in larger groups, for example through sharing of food or grooming interactions (Dunbar 1991). Third, social groups represent natural habitat patches for parasites, linked through dispersal events, which diminishes the importance of overall population size for disease spread relative to local group size (McCallum and Dobson 2002). Finally, the size and composition of social groups affect other aspects of social systems, such as mating system and the existence of dominance hierarchies (Kappeler and van Schaik 2002).

In contrast to the usual prediction that group size correlates positively with disease risk, several authors have argued that sociality should reduce the risk of acquiring directly transmitted parasites (Watve and Jog 1997; Wilson et al. 2003). These conclusions are based on theoretical models showing that increased clustering reduces disease risk if dispersal among groups is low (Fig. 3.8). As individuals become more tightly clumped into relatively permanent groups, infections could be effectively "quarantined" into patches, and parasites are therefore less likely to establish in these structured metapopulations (Hess 1996). However, although population sub-structuring could reduce the spread of disease at the population level, as compared to panmictic mixing, once clumping occurs disease risk might still be expected to increase in larger groups.

Finally, vector-borne diseases could be positively or negatively influenced by group size, with effects depending on vector behavior and biology. Thus, mobile parasites that actively search for hosts, such as flying arthropods, could be preferentially attracted to larger groups, perhaps through greater emission of cues used by arthropods to locate hosts (Davies et al. 1991; Nunn and Heymann 2005). Alternatively, living in a larger group could help animals avoid flying vectors; if the probability of locating a group does not increase proportionally with group size or lead to higher biting rates by individual insects, individual infection risk should be lower in larger groups. Mooring and Hart (1992) refer to this process as the

Clustering coefficient (Q)

Fig. 3.8 Host clustering and sociality may reduce disease risk by subdividing the population and reducing parasite spread. This plot, from Wilson et al. 2003, shows how increased clustering (Q) decreases per capita infection risk in a simulation study. At Q = 0, reproduction occurs at random to any site within the population, and at Q = 1, all reproduction is local, which is equivalent to a highly structured host population in which individuals live in permanent groups. Line represents the best-fit exponential function. From Wilson, K., R. Knell, M. Boots, and J. Koch-Osborne (2003). Group living and investment in immune defence: An interspecific analysis. Journal of Animal Ecology, 72, 133-143. Permission granted by Blackwell publishing.

Clustering coefficient (Q)

Fig. 3.8 Host clustering and sociality may reduce disease risk by subdividing the population and reducing parasite spread. This plot, from Wilson et al. 2003, shows how increased clustering (Q) decreases per capita infection risk in a simulation study. At Q = 0, reproduction occurs at random to any site within the population, and at Q = 1, all reproduction is local, which is equivalent to a highly structured host population in which individuals live in permanent groups. Line represents the best-fit exponential function. From Wilson, K., R. Knell, M. Boots, and J. Koch-Osborne (2003). Group living and investment in immune defence: An interspecific analysis. Journal of Animal Ecology, 72, 133-143. Permission granted by Blackwell publishing.

encounter-dilution effect, suggesting that feeding characteristics of flying insects can exert different effects on the grouping behavior of animals. Thus, host grouping could reduce attacks by blood-sucking flies because such micro-predators typically are satiated after one or two blood meals, whereas warble flies can deposit eggs on multiple animals, with grouping providing fewer benefits to individual hosts (Mooring and Hart 1992; Hart 1994).

In summary, a variety of mechanisms are likely to play a role in generating correlations between group size and disease risk, with contact among individuals, contact among groups, parasite transmission mode, and vector behavior paramount among these factors.

3.3.3.1 Empirical evidence for an effect of group size: contagious parasites

Empirical tests of the link between group size and infection with directly transmitted parasites have produced mixed results (Krause and Ruxton 2002). Multiple field studies of mammals support this hypothesis (Kunz 1976; Freeland 1979; Hoogland 1979; Wilkinson 1985; Brown and Brown 1986; Shields and Crook 1987; Hoogland 1995). On the other hand, some field studies of non-primate mammals failed to find a significant association between group size and parasite risk (e.g. Arnold and Lichtenstein 1993), and probably many other non-significant results remain unpublished. In an attempt to synthesize the results of many field tests, a study spanning insects, birds, and mammals showed that links between group size and parasitism depend on parasite transmission mode (Côté and Poulin 1995). The authors classified parasites into two categories: those spread directly from host-to-host or through intervening substrates (contagious parasites), and parasites that actively search for hosts in water or air (mobile parasites). Using meta-analysis techniques, Côté and Poulin (1995) found a positive association between group size and parasitism for contagious parasites.

Several field studies of primates have tested for an effect of group size on patterns of parasitism. In a classic study, Freeland (1979) found an association between group size and the number of intestinal protozoan species in mangabeys (Cercocebus albigena) at Kibale. Similarly, McGrew et al. (1989a) found a positive trend between nematode infections and group size in baboons at Gombe (n = 3 groups). However, comparative studies in primates have so far revealed few links between social group size and disease risk. Examples include tests of parasite species richness using data on protozoa, helminths, and viruses (Nunn et al. 2003a), and studies of immune system parameters involving relative spleen size (Nunn 2002b) and white blood cell counts (Nunn et al. 2000; Nunn 2002a; Semple et al. 2002). Two studies of helminth species richness in anthropoid primates showed limited support for an effect of group size in primates, but these results became non-significant once phylogeny was taken into account (Nunn et al. 2003a; Vitone et al. 2004). Research on parasite richness in primates has generally focused on taxonomic groups of parasites without regard to transmission mode; thus, future studies should investigate patterns of species richness and prevalence more directly within transmission mode categories, particularly among socially transmitted parasites.

3.3.3.2 Empirical evidence for an effect of group size: vector-borne parasites

In their meta-analysis, Côté and Poulin (1995) found that the intensity of infection with mobile parasites, such as biting flies, showed a negative association with host group size, indicating that animals can lower their individual risk of infection by living in larger groups (e.g. Rutberg 1987; Ralley et al. 1993). Analyses of primate vectors and vector-borne diseases have produced some different patterns. Thus, in a comparative study of 25 species of New World primates, Davies et al. (1991) found that malaria prevalence increased with group size. This result was confirmed in a phylogenetic comparative study based on an updated dataset with the same clade of primates (Nunn and Heymann 2005; Fig. 3.9). Because arthropod vectors spread malaria, these results contradict predictions that group size reduces prevalence and individual infection risk from mobile parasites, possibly because larger groups attract more flying insects.

In contrast, Freeland (1977) argued that the risk of mosquito attacks best explained the timing of polyspecific associations in primates at Kibale, to the exclusion of alternative explanations involving predation and activity levels (see Fig. 1.3). To measure rates of biting fly attacks, Freeland (1977) used data on mosquito activity at Kibale and another field site in Uganda. He found that the hourly occurrence of polyspecific associations correlated positively with mosquito activity levels (see Fig. 1.3), but polyspecific associations were unrelated to rates of eagle attacks (although the sample size of predator attacks was small, with only 18 observed attempts over a nine-month period). The idea that associations among multiple host

Group size

Fig. 3.9 Malaria prevalence in Neotropical primates in relation to group size. Plots show phylogenetically independent contrasts. Evolutionary transitions in group size are positively correlated with transitions in malaria prevalence (t = 4.25, p < 0.001). Results remained significant when using two different phylogenies and three sets of branch lengths, and when transitions to sleeping in closed microhabitats were excluded (see Chapter 5). Data from Nunn and Heymann (2005).

Group size

Fig. 3.9 Malaria prevalence in Neotropical primates in relation to group size. Plots show phylogenetically independent contrasts. Evolutionary transitions in group size are positively correlated with transitions in malaria prevalence (t = 4.25, p < 0.001). Results remained significant when using two different phylogenies and three sets of branch lengths, and when transitions to sleeping in closed microhabitats were excluded (see Chapter 5). Data from Nunn and Heymann (2005).

species can lower the risk of infection from vector-borne diseases is consistent with the outcome of one recent modeling study that showed how vulnerable hosts might be protected from pathogen-driven extinction by the presence of alternative host species (Rudolf and Antonovics 2005). Surprisingly, however, Freeland's conclusions have not been investigated in follow-up studies, and most researchers have focused on other ecological factors as drivers of polyspecific associations, such as foraging or predation benefits (Waser 1987).

3.3.3.3 Social status and individual disease risk

Among individuals, variation in social rank could influence patterns of parasitism. In terms of encounter probabilities, higher status or rank might come at the cost of greater parasitism, as dominant individuals often experience increased mating opportunities and more frequent aggressive interactions. Similarly, socially dominant hosts that forage without restriction could ingest more parasites, just as dominant males that mate with a greater number of partners should be exposed to more STDs (see Chapter 5; Graves and Duvall 1995; Thrall et al. 2000). Thus, in general we expect that encounter probabilities will lead to higher infection rates in more dominant individuals. One possible exception could occur when lower-ranking hosts are forced to use lower quality habitats that might contain more parasites.

Infection probabilities following encounters with parasites produce less clear-cut predictions (Table 3.3). In some cases, more dominant males may suffer to a greater extent from the immunosuppressive effects of testosterone and other hormones, especially in unstable dominance hierarchies (Folstad and Karter 1992; Dixson 1998; Bercovitch and Ziegler 2002). Alternatively, stress in low ranking animals could increase disease risk through modulation of immune defenses (Lloyd 1995; Cohen 1999). Stressful effects of hormones, such as cortisol, may depend on dominance rank and opportunities for kin support (Abbott et al. 2003). Finally, higher dominance rank could improve access to resources that boost overall condition and immunocompetence, leading to better anti-parasite defenses among higher-ranking individuals and therefore lower prevalence of infection.

Thus, as summarized in Table 3.3, higher-ranking individuals should be exposed to a greater number and diversity of parasites, and following exposure, infection probability could augment or offset the encounter probability. Consistent with these diverse expectations, conflicting or ambiguous empirical patterns have been documented in primates (Table 3.4). In their study of yellow baboons, for example, Hausfater and Watson (1976) found that higher-ranking animals expressed increased output of helminth eggs, with the effect more pronounced in males than in females. This result was supported in a later study of the same population using larger sample sizes (Meade 1984). More recent studies of olive baboons, however, found no association between social rank and measures of intestinal helminth infection (Müller-Graf et al. 1996b). Other studies showed that lower-ranking individuals experienced increased disease risk, measured as parasite intensity and impacts on host fitness, including an experimental study of male long-tailed macaques

Table 3.3 Dominance rank and disease risk: roles of encounter and infection probabilities

Variable or effect

Association between higher rank and parasitism

Encounter probability: socially dominant individuals are Positive expected to contact more parasites through better access to food, water, and other resources.

Encounter probability: dominant individuals may experience Positive increased social and mating contact and therefore are more likely to be exposed to parasites.

Infection probability: dominant individuals may experience Positive immunosuppressive effects of testosterone and stress.

Infection probability: improved access to resources may Negative strengthen immune function.

Table 3.4 Social status and parasitism in primates

Host

Parasite(s)

Rank class Notes with greater parasitism

Reference

Papio Two nematode High cynocephalus genera

Papio anubis Six groups No effect of helminths

Cercopithecus Unknown Low aethiops

Papio anubis Lice nits, possibly Low Pedicinus hamadryas

Higher-ranking individuals shed more eggs, with effects more pronounced in males than females.

No association for multiple measures of parasitism, and in males and females.

Lower-ranking individuals were more likely to die from exposure to infectious disease.

Among adults, nits were found more often on females from low-ranking families.

Hausfater and Watson 1976; Meade 1984

Müller-Graf et al. 1996

Cheney et al. 1988

Eley et al. 1989

(Macaca fascicularis) Cohen et al. 1997; Cohen 1999). In the wild, Cheney et al. (1988) found that parasites have a more devastating effect on lower-ranking vervet monkeys (Cercopithecus aethiops). Similarly, lice nits were found more commonly on female olive baboons from lower-ranking families (Eley et al. 1989).

An interesting complication is that parasitism could influence social dominance (rather than vice versa), so that heavily parasitized hosts should also be less able to achieve high dominance rank. Such an effect was suggested for the debilitating effects of cestode infections in geladas (Theropithcus gelada) (Ohsawa 1979). Discerning the direction of cause-and-effect for parasitism and social rank requires experimental manipulations to demonstrate costs of parasitism in terms of failure to achieve high rank. Thus, Freeland (1981b) found that male mice experimentally infected with the nematode Heligmosomoides polygyrus failed to become dominant, but only at the highest inoculation levels (250 larvae per host). Similar results were obtained in an independent experiment using the nematode Trichinella spiralis (Rau 1983).

In summary, the uncertain association between social rank and disease risk in primates probably reflects multiple mechanisms by which social dominance affects exposure and susceptibility to parasites, combined with the fact that we lack a firm understanding of how parasitism could influence dominance rank itself. Future studies that attempt to separate the effects of encounter and infection probabilities, as well as measures of host stress, are needed to reconcile the diverse results in Table 3.4.

3.3.4 Reproduction, mating behavior, and sex differences

3.3.4.1 Reproductive status and breeding effort

Reproduction is a costly activity, and breeding season stress could reduce immune system responsiveness, particularly when resources are limited (Sheldon and Verhulst 1996; Klein and Nelson 1999). Increased reproductive effort in several bird species has been shown to correlate with higher parasite burdens and lower antibody production and cell-mediated immunity (Hillgarth and Wingfield 1997; Duckworth et al. 2001; Moreno et al. 2001; M0ller and Petrie 2002). In primates, males might experience stress from testosterone and mating displays, and among primate species without male parental care, females could exhibit breeding season stress from pregnancy, lactation, and energy devoted to offspring care. Thus, Festa-Bianchet (1989) showed that lactating bighorn sheep (Ovis canadensis) had higher levels of lungworm infection than non-lactating ewes (see also O'Sullivan and Donald 1970). Ewes that raised sons, which are probably more costly to produce than daughters due to extreme sexual dimorphism, had higher levels of infection than those raising daughters (Festa-Bianchet 1989). Pregnant females might also be at greater risk of acquiring parasites during the period of parturition, as mammals have been shown to lower their own immunity during gestation and birth (Lloyd 1983). This probably reduces harm to the fetus, but could also increase the susceptibility of females to infection during or immediately following pregnancy (Cattadori et al. 2005).

Few studies have examined parasitism relative to host reproductive activity in primates, but the limited evidence fails to support the prediction that parasite risk increases during gestation or lactation. Yellow baboon females at Amboseli that were lactating or not cycling (and thus possibly pregnant) shed fewer worm eggs than females showing estrous cycles (Hausfater and Watson 1976), although a later study found higher parasite levels among pregnant females in the same population (Meade 1984). Similarly, Müller-Graf et al. (1996, 1997) found that reproductive status was unrelated to the prevalence of intestinal parasites and schistosome infections in female baboons at Gombe, although lactating females showed higher intensity of infection with Trichuris sp. Interestingly, pregnant females exhibited the lowest level of infection. Among female howler monkeys, those with dependent offspring had fewer botfly larvae than females without infants, at least toward the end of the dry season (Smith 1977). Patterns that are opposite to predictions might be caused by greater investment in behavioral and immune defenses among reproductive females, or by negative effects of infection on female reproduction. Further field and experimental research on parasite risk among lactating and cycling females could shed more light on these questions, and on the more general effect of mating season on patterns of parasitism.

3.3.4.2 Mating promiscuity

Sexual contact provides an effective means for parasite transmission, as revealed by the remarkable diversity of STDs in humans (Holmes et al. 1999). Risks of acquiring STDs should be higher in animals with promiscuous mating systems (Loehle 1995; Lockhart et al. 1996; Heymann 1999; Nunn et al. 2000) or in populations with higher variance in male mating success (i.e. mating skew; Thrall et al. 2000). The latter effect arises because a few individuals with large numbers of mating partners can serve as loci ("super-spreaders") for infections to spread through populations (see Chapter 4 and Anderson 1999). Finally, STDs may be more common relative to other infectious diseases in species living solitarily at low density, as mating is one of the few times in which social contact occurs (Smith and Dobson 1992; Thrall et al. 1998).

Is STD risk greater in species characterized by promiscuous mating contact? Although more than 20% of primate species have been classified as monogamous (C. Nunn, unpublished comparative database), the vast majority of reported STDs have been documented in non-monogamous primate species (Table 3.5 and Nunn and Altizer 2004). However, this apparent pattern could also reflect sampling bias if researchers tend to search for STDs in more promiscuous primate species.

Nunn and colleagues (2000, 2002a) conducted comparative tests across a diverse assemblage of primates to assess whether baseline leukocyte counts were associated with mating promiscuity. Consistent with predictions, primate lineages characterized as being more promiscuous exhibited higher leukocyte counts in phylogenetic comparative tests (see Fig. 1.2). These results were upheld when using different measures of promiscuity, after controlling for additional variables, and when limiting the analysis to adult females or males only. More recently, a similar pattern was obtained using an independent dataset on primate leukocyte counts (Anderson et al. 2004) and in an analysis of carnivores (Nunn et al. 2003b). In Chapter 5, we consider the mechanisms that might underlie this pattern.

Table 3.5 Sexually transmitted parasites documented in wild primates

Genus1

Parasite(s) exhibiting probable sexual transmission2

Mating system

Alouatta palliata Ateles fusciceps Callithrix jacchus

Cebus capucinus Cercocebus (3) Cercopithecus (10)

Colobus guereza

Erythrocebus patas Gorilla gorilla Hylobates (1-2) Macaca (10 + ) Mandrillus (2)

Miopithecus talapoin Pan troglodytes

Pongo pygmaeus Presbytis (2) Procolobus verus Theropithecus gelada

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