Introduction

The previous chapter reviewed the incredible diversity of parasites found in primates and highlighted some of the ways that parasites are transmitted from host-to-host. This chapter addresses a different question: how do primate behaviors, life history, and ecology influence disease risk? To illustrate the links between primate traits and disease risk, we begin by describing three hypothetical examples that aim to capture how infections might spread through primate populations.

First, consider a male ring-tailed lemur (Lemur catta, Fig. 3.1) from Madagascar. Males of this species move between social groups upon reaching maturity, leaving

Fig. 3.1 A male ringtailed lemur at the Duke University Primate Center using his antebrachial (carpal) glands to mark a sapling. Photo by C. Nunn.

Fig. 3.2 Two ringtailed lemurs at the Duke University Primate Center performing allogroom-ing, with a juvenile about to join in. Ringtailed lemurs use their mouths to groom the fur of other individuals and pairs of individuals often perform the grooming activities simultaneously.

Photo by C. Nunn.

Fig. 3.2 Two ringtailed lemurs at the Duke University Primate Center performing allogroom-ing, with a juvenile about to join in. Ringtailed lemurs use their mouths to groom the fur of other individuals and pairs of individuals often perform the grooming activities simultaneously.

Photo by C. Nunn.

their natal group to search for breeding opportunities in other groups (Jones 1983; Pereira and Weiss 1991). The grooming network of juvenile males within their natal ranges includes their mothers and other juveniles (Kappeler 1993; Nakamichi and Koyama 1997). Ring-tailed lemurs groom each other with their mouths (allogrooming, Jolly 1966; Fig. 3.2), an activity that provides hygienic benefits but also facilitates parasite transmission through contact with infectious stages caught in the fur or from saliva left by previous grooming partners. Close proximity during grooming could also facilitate the spread of respiratory pathogens. In socially structured primates like these lemurs, contact within groups provides a network for the spread of pathogens, and male dispersal to new groups serves as a conduit for among-group parasite transmission. Thus, patterns of group fidelity and host dispersal are central to understanding the establishment and spread of directly transmitted parasites (Freeland 1979).

As a second example, consider a female mantled howler monkey (Alouatta palliata) living in Costa Rica (Fig. 3.3). Howler monkeys are exposed to an incredible array of vector-borne parasites, such as Plasmodium brasilianum (a relative of the human malaria parasite) and flaviviruses such as those that cause yellow fever (Galindo and Srihongse 1967; Stuart et al. 1998). These monkeys also suffer from arthropod parasites, including a species of botfly (Alouattamyia baeri, see Fig. 2.10) that specializes on howler monkeys and can contribute toward mortality (Milton 1996). As a result, female reproductive success in mantled howler monkeys is probably tightly linked to avoiding flies, mosquitoes, and other blood-feeding arthropods. How can female monkeys avoid such parasites? Viewing arthropods as micro-predators (see Chapter 1), one behavioral defense is to use predator-avoidance

Fig. 3.3 Mantled howling monkey from Costa Rica. Image courtesy of K. Glander, Duke

University.

Fig. 3.3 Mantled howling monkey from Costa Rica. Image courtesy of K. Glander, Duke

University.

tactics, such as living in a group (Hamilton 1971; Janson 1992), to lessen the individual risk of being attacked by an arthropod (the "encounter-dilution" effect, Mooring and Hart 1992). Females in larger groups therefore can reduce risk from vector-borne diseases, but this strategy could come at the cost of increased prevalence of socially transmitted infections in these larger groups. At smaller spatial and temporal scales, females actively defend themselves by using specific arthropod-avoidance behaviors such as slapping at insects to shoo them away. But these behavioral defenses can be energetically costly (Dudley and Milton 1990) and might take away from time spent resting, foraging, or socializing. Thus, living in social groups and actively avoiding mobile arthropods represent key behavioral mechanisms used by primates to limit their risk of contracting a vector-borne disease, but these behaviors are themselves associated with energetic or opportunity costs and greater risk of acquiring other pathogens.

Finally, consider an adult female bonobo (Pan paniscus, Fig. 3.4). In many ways, bonobos are similar to chimpanzees (P. troglodytes), but bonobos display extremely promiscuous behavior (Wrangham 1993). A female bonobo typically mates with several males and may also rub genitals with other females in the community (Manson et al. 1997). The bonobos' promiscuous hetero- and homosexual behaviors should provide a highly efficient network for the spread of sexually transmitted diseases (STDs). Surprisingly little is known about STDs in bonobos (Van Brussel et al. 1998), but data are available on probable STDs in other apes (Eberle 1992; Verschoor et al. 1998; Gao et al. 1999; Santiago et al. 2002) and monkeys (Lockhart et al. 1996). Because the transmission of STDs should be tightly linked to host mating contacts, bonobos should harbor a variety of STDs that could play an important role in their reproductive success and conservation. Alternatively, the

Fig. 3.4 Bonobos grooming, with infant in background. Photographed by F. White,

University of Oregon.

Fig. 3.4 Bonobos grooming, with infant in background. Photographed by F. White,

University of Oregon.

extreme promiscuity of bonobos might have followed from the evolution of effective behavioral and immune defenses in this host species, or other factors that caused the loss of STDs in wild bonobo populations.

These examples reveal some of the many links between parasite transmission and host behavior and ecology. Obviously even simple questions become complicated when the same activities—such as grooming or clustering in groups—lower the risk of certain parasite types but increase exposure to others. To make progress in identifying the links between parasites and primate socioecology, we need a conceptual framework that identifies the primary host traits that influence disease risk for parasites with different transmission modes. For example, lemur social groups probably serve as metapopulations for directly transmitted parasites, but what about parasites that use invertebrates as intermediate hosts or vectors, in which host population sub-structuring might pose less of a barrier to pathogen spread? In the example of howler monkeys, how are the benefits of living in a larger group to reduce risks of biting fly attacks balanced against the costs of acquiring infectious diseases spread through social contact? Do bonobos possess effective behavioral defenses to STDs, such as choosing healthy mates and post-copulatory genital grooming (Hart et al. 1987; Nunn 2003)? If so, do these behavioral defenses influence the characteristics of STDs, such as the expression of outward signs of infection (Knell 1999)?

A comprehensive framework for studying disease risk is needed to elucidate mechanisms underlying patterns of parasitism and to identify particular host defenses to infectious disease. To develop such a framework, we must first identify

Box 3.1 Chapter outline (specific hypotheses are summarized in Table 3.1) Background concepts

• Encounter and infection probability (Section 3.2.1)

• Formulating hypotheses at individual and comparative levels (3.2.2)

Host traits and disease risk

• Body mass, life history, and individual age (3.3.1)

• Host population size and density (3.3.2)

• Social organization, group size, and dominance rank (3.3.3)

• Reproduction, mating behavior, and sex differences in parasitism (3.3.4)

• Ranging patterns, substrate use, and diet (3.3.5)

• Environmental factors and seasonality (3.3.6)

Synthesis and conclusions (3.4)

the combinations of host and parasite traits that impact disease risk. The goal of this chapter is to identify these traits, their interactions with parasite characteristics, and the evidence for each trait as influencing disease risk. Later chapters build on this framework with more sophisticated theoretical approaches. Because this chapter might be consulted at later stages, we provide an outline of the major classes of host traits examined in this chapter (Box 3.1) and a table that summarizes the key predictions (Table 3.1). Before moving on to consider these traits on a case-by-case basis, we review background concepts related to the occurrence of particular host-parasite combinations and the levels at which different traits may operate.

Was this article helpful?

0 0

Post a comment