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Black and Gold Howler Monkeys (Alouatta Caraya) As Sentinels of Ecosystem Health: Patterns of Zoonotic Protozoa Infection Relative to Degree of Human–Primate Contact

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Black and Gold Howler Monkeys (Alouatta Caraya) As Sentinels of Ecosystem Health: Patterns of Zoonotic Protozoa Infection Relative to Degree of Human–Primate Contact American Journal of Primatology 73:75–83 (2011) RESEARCH ARTICLE Black and Gold Howler Monkeys (Alouatta caraya) as Sentinels of Ecosystem Health: Patterns of Zoonotic Protozoa Infection Relative to Degree of Human–Primate Contact MARTIN M. KOWALEWSKI1, JOHANNA S. SALZER2, JOSEPH C. DEUTSCH3, MARIANA RAN˜ O1, 3 2,4Ã MARK S. KUHLENSCHMIDT , AND THOMAS R. GILLESPIE 1Estacio´n Biolo´gica de Usos Mu´ltiples de Corrientes (EBCo), Museo Argentino de Ciencias Naturales-CONICET, Argentina 2Department of Environmental Studies and Program in Population Biology, Ecology, and Evolution, Emory University, Atlanta, Georgia 3Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois 4Department of Environmental and Occupational Health, Rollins School of Public Health, Emory University, Atlanta, Georgia Exponential expansion of human populations and human activities within primate habitats has resulted in high potential for pathogen exchange creating challenges for biodiversity conservation and global health. Under such conditions, resilient habitat generalists such as black and gold howler monkeys (Alouatta caraya) may act as effective sentinels to overall ecosystem health and alert us to impending epidemics in the human population. To better understand this potential, we examined noninvasively collected fecal samples from black and gold howler monkeys from remote, rural, and village populations in Northern Argentina. We examined all samples (n 5 90) for the zoonotic protozoa Cryptosporidium sp. and Giardia sp. via immunofluorescent antibody (IFA) detection. All samples were negative for Cryptosporidium sp. The prevalence of Giardia sp. was significantly higher at the rural site (67%) compared with the remote forest (57%) and village (40%) sites. A lack of Cryptosporidium sp. in all samples examined suggests that this pathogen is not a natural component of the howler parasite communities at these sites and that current land-use patterns and livestock contact are not exposing Argentine howler monkeys to this pathogen. High prevalence of Giardia sp. at all sites suggests that howler monkeys may serve as a viable reservoir for Giardia. Significantly higher prevalence of Giardia sp. at the rural site, where primate–livestock contact is highest, suggests the presence of multiple Giardia clades or increased exposure to Giardia through repeated zoonotic transmission among nonhuman primates, livestock, and/or people. These results highlight the need for future research into the epidemiology, cross-species transmission ecology, and clinical consequences of Giardia and other infectious agents not only in humans and livestock, but also in the wild animals that share their environments. Am. J. Primatol. 73:75–83, 2011. r 2010 Wiley-Liss, Inc. Key words: Cryptosporidium; disturbance ecology; Giardia;neglectedpathogens;primate;Zoonoses INTRODUCTION primates to serve as sentinels, alerting us before pathogens reach semi-urban or urban areas. Exponential expansion of human populations The forests of Northern Argentina provide an and human activities within primate habitats has ideal locale for examining issues related to pathogen resulted in high potential for multi-directional exchange between people, nonhuman primates, and pathogen exchange creating challenges for biodiver- sity conservation and global health [Gillespie et al., 2008]. Associated landscape-level disturbance may Contract grant sponsor: NIH; Contract grant number: T35 2006; exacerbate pathogen transmission by affecting the Contract grant sponsors: The Wenner Gren Foundation; Post- distribution and behavior of primates [Gillespie & Ph.D. Research Grant; Contract grant number: 7622; Contract Chapman, 2006, 2008; Gillespie et al., 2005; Nunn & grant sponsor: Conservation Medicine Center of Chicago. Altizer, 2006], as well as vectors of infectious diseases ÃCorrespondence to: Thomas R. Gillespie, E510 Math and such as yellow fever, dengue, and malaria [Altizer Science Center, 400 Dowman Drive, Emory University, Atlanta, Georgia 30322. E-mail: [email protected] et al., 2006; Hay et al., 2002]. In this regard, studies of Received 28 September 2009; revised 26 December 2009; nonhuman primates with the ability to survive in revision accepted 26 December 2009 moderately disturbed habitats are of great impor- DOI 10.1002/ajp.20803 tance for understanding the dynamics of infectious Published online 18 January 2010 in Wiley Online Library (wiley disease transmission and to evaluate the capacity of onlinelibrary.com). r 2010 Wiley-Liss, Inc. 76 / Kowalewski et al. livestock. Here, commercial agriculture (i.e., soy recent genetic differentiation among groups and a plantations) and forest exploitation have profoundly lower genetic heterozygosity, potentially due to changed the composition of forests, eliminating the limitations in dispersal opportunities [Oklander, hardiest and most economically profitable forest tree 2007]. The impacts of habitat alteration on nonhu- species [Zunino & Kowalewski, 2008]. Clearing man primate populations occur at the individual, entire forests for agriculture and establishing exotic, group, and population level. Successful mediation of fast-growing pastures are also contributing to rapid these threats requires repeated evaluation of genetic landscape change in this region. The effects of these diversity, health, stress, behavior, and diet. A study changes on wildlife populations remain largely on red colobus (Piliocolobus tephrosceles) revealed unknown. In Argentina, black and gold howler the synergistic affects of food availability, cortisol monkeys, Alouatta caraya, account for the highest levels, and parasite infections on the abundance of proportion of biomass of arboreal mammals and this species [Chapman et al., 2006]. Case studies of these monkeys often cope well with moderate various species from sites around the world will deforestation [Zunino et al., 2007]. The high degree improve our understanding of the multifactorial of phenotypic plasticity present in this species make process that anthropogenic disturbances can initiate black and gold howler monkeys a valuable species to at different levels. test and evaluate current ideas of conservation In this study we examine patterns of infection related to the dynamics of emergent and re-emergent with the zoonotic protozoa, Giardia, and Cryptospor- diseases [Kowalewski & Gillespie, 2009], since more idium, in populations of black and gold howler plastic species are expected to occupy and success- monkeys living at variable levels of contact with fully exploit a wider range of ecological conditions, humans: remote, rural, and village. These protozoa leading to greater resilience to habitat seasonality infect vertebrates, including wildlife, livestock, and and habitat modification compared with other taxa humans [Hill, 2001; McGlade et al., 2003; Volota˜o [Miner et al., 2005]. Howlers are classified as et al., 2008]. The protozoa life cycle consists of colonizers [Crockett, 1998; Crockett & Eisenberg, fecal–oral transmission of Giardia cysts or Cryptos- 1987; Eisenberg et al., 1972] due to their ability to poridium oocysts (infective stage), typically via adapt and survive in modified environments [Bicca- contaminated water and food. Within the host Marques, 2003; Clarke et al., 2002a]. This ability animal, the life cycle of the protozoa continues as to survive in variable environments including habi- the cysts or oocysts develop into trophozoites. The tats that bring them into contact with humans trophozoites infect cells within an animal host’s [Cabral et al., 2005; Estrada et al., 2006; Mun˜oz duodenum; often leading to severe diarrhea [Thompson, et al., 2006] or increase their terrestrial travel 2004]. Giardia is cosmopolitan and constitutes a [Kowalewski et al., 1995; Pozo-Montuy & Serio- recognized waterborne infection for humans and Silva, 2006; Young, 1981], make howlers an excellent animals, responsible for well over one billion cases of model to study the dynamics of infectious disease human diarrheal disease annually [Crompton, 2000; transmission among wild primates, humans, and Teodorovic et al., 2007; WHO/UNICEF, 2000]. domestic animals. Giardiasis is now considered by the World Health Although black and gold howlers, much like Organization to be a ‘‘neglected disease,’’ due to its other species of Alouatta, seem to be resilient to ubiquity in equatorial latitudes, its chronic detri- variable levels of habitat degradation in terms of mental health effects (especially in children), its population numbers [Estrada et al., 2006; Zunino propensity to infect economically disadvantaged et al., 2007], a finer-scale analysis reveals a different populations, and the paradoxical availability of scenario. As in colobine species [Gillespie & Chapman, relatively inexpensive and effective pharmaceuticals 2006, 2008], howler populations living in fragmented for its treatment [Savioli et al., 2006]. In Latin forests seem to be carrying a more diverse commu- America almost 15% of the rural population is nity of parasites [Kowalewski & Gillespie, unpub- infected with Giardia [Atı´as, 1999]. In Argentina, lished data; Santa Cruz et al., 2000]. Oklander [2007] two human studies showed a prevalence of 10% in revealed another trend in howler populations living urban areas, 34% in small towns (same as villages in fragmented forests in Northern Argentina (the considered in our study) [Gamboa et al., 2003], and same study site of this article—EBCo-, see descrip- 4% in rural areas [Minvielle
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