Chapter 17 Ecological and Anthropogenic Influences on Patterns of Parasitism in Free-Ranging Primates: A Meta-analysis of the Genus Alouatta Martin M. Kowalewski and Thomas R. Gillespie 17.1 Introduction Parasites play a central role in tropical ecosystems, affecting the ecology and evolution of species interactions, host population growth and regulation, and com- munity biodiversity (Esch and Fernandez 1993; Hudson, Dobson and Newborn 1998; Hochachka and Dhondt 2000; Hudson et al. 2002). Our understanding of how nat- ural and anthropogenic factors affect host-parasite dynamics in free-ranging pri- mate populations (Gillespie, Chapman and Greiner 2005a; Gillespie, Greiner and Chapman 2005b; Gillespie and Chapman 2006) and the relationship between wild primates and human health in rural or remote areas (McGrew et al. 1989; Stuart et al. 1990; Muller-Graf, Collins and Woolhouse 1997; Gillespie et al. 2005b; Pedersen et al. 2005) remain largely unexplored. The majority of emerging infec- tious diseases are zoonotic – easily transferred among humans, wildlife, and domes- ticated animals – (Nunn and Altizer 2006). For example, Taylor, Latham and Woolhouse (2001) found that 61% of human pathogens are shared with animal hosts. Identifying general principles governing parasite occurrence and prevalence is critical for planning animal conservation and protecting human health (Nunn et al. 2003). In this review, we examine how various ecological and anthropogenic factors affect patterns of parasitism in free-ranging howler monkeys (Genus Alouatta). 17.1.1 Evidence of the Relationships Between Howlers and Parasitic Diseases in South America The genus Alouatta is the most geographically widespread non-human primate in South America, with 8 of 10 Alouatta species ranging from Northern Colombia M.M. Kowalewski (B) Estacion Biologica Corrientes-MACN, Corrientes, Argentina; Department of Anthropology, University of Illinois, Urbana-Champaign, IL, USA e-mail: [email protected] P.A. Garber et al. (eds.), South American Primates, Developments in Primatology: 433 Progress and Prospects, DOI 10.1007/978-0-387-78705-3 17, C Springer Science+Business Media, LLC 2009 434 M.M. Kowalewski and T.R. Gillespie to Argentina (Cort´es-Ortiz et al. 2003). Howlers are classified as colonizers (Eisenberg 1972; Crockett 1998) due to their ability to adapt and survive in modi- fied environments (Clarke et al. 2002; Bicca-Marques 2003; Zunino et al. 2007). In addition, in contrast to other New World primate taxa, data on patterns of parasitism in free-ranging howlers are available from variable environments throughout the geographic range of the Genus. This availability of published data on patterns of parasitism, coupled with their ability to survive in variable environments includ- ing those that bring them into increasing contact with human communities, make howlers an excellent model to study the dynamics of infectious disease transmission among wild primates, humans and domestic animals. Howlers are known to be host to bacteria, protozoa, viruses, fungi, helminthes, and arthropods that also infect livestock and humans (Stuart et al. 1998). This shared susceptibility to infection has the capacity to lead to cross-species transmission in disturbed forest systems where howlers experience higher temporal and spatial over- lap with livestock and humans. Howler habitation of forest patches within plantations and cattle pastures or in close proximity to human settlements (Cabral et al. 2005; Estrada et al. 2006; Mu˜noz et al. 2006); frequent terrestrial travel (Young 1981; Kowalewski, Zunino and Bravo 1995; Delgado 2006; Pozo-Montuy and Serio-Silva 2007); and drinking from rivers and lagoons (Gilbert and Stouffer 1989; Bravo and Sallenave 2003), all increase opportunities for cross-transmission. In this chapter we integrate and compare data from studies on wild Alouatta caraya, A. seniculus, A. guariba,and A. belzebul inhabiting areas of undisturbed continuous forests and areas character- ized by forest fragmentation and other anthropogenic pressure. We use these data to test a series of hypotheses concerning the relationship between habitat attributes and patterns of parasitism, and we consider how these processes may affect howler metapopulations. 17.1.2 Problems with Data Availability on Primates and Parasitic Diseases in South America Information on parasites in New World primates is extremely fragmentary. Reviews have been published on the presence/absence of parasites in howlers, or with refer- ence to howlers as parasite hosts (see Yamashita 1963; Diaz Ungria 1965; Thatcher and Porter 1968; Stuart et al. 1998; Stoner et al. 2005). However, several of these reviews include data on captive or semi-free ranging howlers. Such parasite lists are useful, but are unlikely to reflect the full range of host-parasite interactions in wild populations. Additional data on parasite prevalence in South American primates come from (a) examination of monkeys relocated or rescued from areas flooded by dam projects (see Fandeur et al. 2000; Volney et al. 2002; Duarte et al. 2006), (b) biomedical studies focusing on parasites that produce critical economic losses to human populations such as malaria, yellow fever and toxoplasmosis (Kumm and Laemmert 1950; Deane 1992; Lourenco de Oliveira and Deane 1995; Volney 17 A Meta-analysis of the Genus Alouatta 435 et al. 2002; Vasconcelos et al. 2003; Garcia et al. 2005), and (c) studies of a limited number of primate social groups to compare prevalence and presence of parasites in relation to habitat fragmentation (see Gilbert 1994; Santa-Cruz et al. 2000a,b; Godoy et al. 2004; Martins 2002; Delgado 2006; Kowalewski and Santa-Cruz, unpub. data). 17.1.3 Effect of Deforestation on Parasite Infections Previous studies have shown that disturbance may alter the dynamics of parasite transmission (Gillespie et al. 2005a; Gillespie and Chapman 2006). A direct con- sequence of deforestation and increased fragmentation is the modification of forest structure and composition (Johns and Skorupa 1987; Plumptre and Reynolds 1994; Marsh 2003; Norconk and Grafton 2003; Rivera and Calme 2006). Selective log- ging is associated with the disappearance of species of economic value that may also be important in the diet of primates (Kowalewski and Zunino 1999, Gillespie et al. 2005a). Clear cutting of forests reduces the area of forest coverage drastically. Both selective logging and clear cutting allow the invasion of secondary forest, modifying forest composition and structure (Norconk and Grafton 2003; Zunino et al. 2007). These changes may result in dietary and nutritional stress on primate foragers, negatively affecting immune response and leaving individuals more sus- ceptible to both parasitic infections and infectious diseases (Milton 1996; Solomons and Scott 1994; Chapman et al. in press). It has been shown that some species of primates living in logged forest have higher parasite prevalence and diversity (i.e., Cercopithecus ascanius [Gillespie et al. 2005a]; Alouatta palliata [Stoner 1996]; Alouatta caraya [Santa Cruz et al. 2000a]). Increasing contact between humans and primates and reduction of primate ranging areas result in increasing probabil- ities of infections for both humans and primates (Gillespie 2004, Stoner and Di Perro 2006) 17.1.4 Goals of This Study A more detailed understanding of the relationship between patterns of parasitism and attributes of primate habitat will allow for more effective primate conservation and safeguarding of human and animal health. In this chapter, we take a meta- analysis approach to examine how various factors such as latitude, type of for- est, altitude, annual precipitation, and degree of contact with human settlements affect parasite prevalence in populations of howler monkeys inhabiting different sites across South America. Some of the studies included in our analysis contain data on the prevalence of gastrointestinal, blood and ectoparasites of different par- asite species studied at the same study site during different seasons or years (see Appendix 1). These comparisons are therefore not independent. However, we feel that to exclude non-independent comparisons may bias or limit our results more 436 M.M. Kowalewski and T.R. Gillespie than their inclusion (Hedges and Olkin 1985; Gurevitch et al. 1992; Poulin 1994). Therefore we considered the studies in Appendix 1 in our analysis in order to answer the following questions: Do certain habitat features affect parasite prevalence and diversity in non-human primates across South America? Does the degree of con- tact between humans and nonhuman primates affect parasite prevalence in wild primates? We also compare our howler-specific results with those of Nunn et al. (2005). In a comparison of 330 parasite species from 119 nonhuman primate species hosts, protozoan, but not helminth or virus, species richness was negatively correlated with distance from the equator. They argued that this effect may be caused by a greater abundance of arthropods serving as intermediate hosts in the tropics, as well as climate effects on both vectors and parasites. For example, warmer latitudes are associated with higher vector biting rates and more rapid parasite development (Liang, Linthicum and Gaydos 2002; Nunn et al. 2005). 17.2 Methodology 17.2.1 Meta-analysis: Parameters Used We conducted a systematic review of published literature, dissertations, and per- sonal communications with primate researchers in the field. Appendix 1 provides the following data: species of