The Influence of Human Settlements on the Parasite Community in Two

675 The influence of human settlements on the parasite community in two species of Peruvian tamarin A. WENZ1*, E. W. HEYMANN2,T.N.PETNEY1 and H. F. TARASCHEWSKI1 1 University of Karlsruhe, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany 2 German Primate Center, Department of Behavioural Ecology and Sociobiology, Kellnerweg 4, 37077 Go¨ttingen, Germany (Received 2 June 2009; revised 5 August, 28 August and 30 September 2009; accepted 30 September 2009; first published online 22 December 2009) SUMMARY Although there is a growing recognition that the transfer of diseases between humans and non-human primates can be of great significance for conservation biology, there have been only a few studies focusing on parasites. In this study, saddleback (Saguinus fuscicollis) and moustached tamarin (Saguinus mystax) from the rainforest of the Peruvian lowlands were used as models to determine helminth parasite associations between canopy-dwelling primate species and a nearby human settlement. The human population showed high prevalences of infestation with a number of nematodes, including Ascaris lumbricoides (88.9%), Trichuris trichiura (37%) and hookworms (55.6%). However, the ova of these geohelminths were not detectable in tamarin faeces. Thus, no direct parasite transfer from humans to non-human primates could be documented. However, tamarin groups with more frequent contact to humans and their facilities had significantly higher prevalences and egg output of Prosthenorchis elegans, an important primate pathogen, than a forest group. In contrast, a cestode was significantly more common with more egg output in sylvatic than in human-associated groups. Human alteration of the habitat is likely to play a major role in determining the occurrence, prevalence and intensity of helminth infestation of wild non-human primates. Key words: Peru, primates, parasites, tamarin, Prosthenorchis elegans, humans, synanthropic transmission. INTRODUCTION (Chapman and Peres, 2001; Wolfe et al. 2004). Non- human primates are now commonly forced to live in Infectious disease is listed among the top five causes an anthropogenically disturbed landscape compris- of global species extinctions (Young, 1994; Smith ing farmland, human settlements, forest fragments et al. 2006). Historically, diseases of wildlife have and isolated protected areas (Chapman and Peres, only attracted public attention when domestic ani- 2001). Gillespie and Chapman (2006) found that the mals or human health were involved. However, there index of forest patch degradation and the presence is a growing awareness of the role of pathogens in of humans strongly influenced the prevalence of the population dynamics of wildlife and, in particu- parasitic gastrointestinal nematodes in red colobus lar, endangered species (Daszak et al. 2000; Ko¨ndgen monkeys. This suggests that, as forest fragments et al. 2008). Indeed, disease has become a major con- become smaller and frequency of contact between cern in wildlife conservation, both inside and outside humans and non-human primates becomes higher, of park and reserve boundaries (Daszak et al. 2000; transmission of diseases and pathogens is increasingly Lafferty, 2003; Smith et al. 2006). As a result of the likely. human population explosion, combined with illegal Due to the genetic similarity between humans hunting, and the fragmentation and degradation of and non-human primates, the transmission of patho- formerly natural habitats, wild animals are increas- gens between or among primates is of particular ingly subjected to contact with humans. This situ- significance (Wolfe et al. 1998; Chapman et al. 2005). ation may facilitate disease transmission among Indeed, recent work has shown that non-human humans, livestock and wildlife (Bengis et al. 2002; primate populations harbour a variety of pathogens Woodford et al. 2002). similar to those causing significant disease in humans Although humans have always shared habitats (Leendertz et al. 2006; Chi et al. 2007; Perpens et al. with non-human primates the dynamics of hu- 2007) that may be zoonotic. Such pathogens have man-primate interactions are changing radically already led to major epidemic problems for human health, such as the transfer of HIV viruses to the human population (Daszak et al. 2004). Cross- * Corresponding author: University of Karlsruhe, transmission of parasites to non-human primates Zoological Institute, Department of Ecology and Para- sitology, Kornblumenstrasse 13, 76131 Karlsruhe, has been inferred in a number of African primates Germany. Tel: +49 721 6084717. Fax: +49 721 6087655. (Mudakikwa et al. 1998; Graczyk et al. 2001; Lilly E-mail: [email protected] et al. 2002). Parasitology (2010), 137, 675–684. f Cambridge University Press 2009 doi:10.1017/S0031182009991570 A. Wenz and others 676 However, finding morphologically identical nema- Diamante. The home range of this group reached to todes in human and wild primates should be treated the houses of the villagers and included the village with caution. For example, Oesophagostomum bifur- toilet, the rubbish dump and fields planted with cum from humans were genetically distinct from yucca, plantains and other fruit. In addition, parts of those harboured by some non-human primates, and the tamarin homerange consist of secondary forest. these genetic differences were predicted to be as- Villagers cross the homerange every day to get to sociated with distinct transmission patterns (de their crops and to collect wood. This tamarin group Gruijter et al. 2005; Gasser, 2009). Still, very little is designated group D. The second human contact information is available on the extent of transfer of troop had its homerange around the EBQB, which is pathogens between humans and non-human pri- situated in a clearing, with a minimum distance of 5 mates. In particular, limited information is available metres to the field station. There are no crops in this on the prevalence of intestinal parasitism in feral area, but the tamarin’s range includes the station neotropical primates (Michaud et al. 2003; Phillips rubbish dump and the toilet. The number of occu- et al. 2004). Almost nothing is known about the in- pants of the EBQB varies between 2 and up to 20 fluence of human settlements bordering the natural people, and some of the villagers from Diamante habitats of non-human primates on the gastrointes- work at the station. The sampled tamarin group is tinal parasites of primates. The primary objective of designated group 1. The other groups lived deeper in this study was to determine the influence of human the forest with no contact to humans or their facilities contact and habitat modification on the presence of except for the observers watching them for a variable gastrointestinal parasites in two tamarin species from number of days each month (groups 2 and 3). For size a tropical rainforest area in Peru, the saddleback and species composition of the groups see Table 2. tamarin (Saguinus fuscicollis) and the moustached tamarin (Saguinus mystax). Collection and examination of faecal samples Fresh faecal droppings from all group members were MATERIALS AND METHODS collected during the dry season between July and Study site September 2007 by following the groups during their whole activity period (06.00–16.30). Faecal samples The study was conducted in the Amazonian lowlands were gathered directly after defecation. Locality, of northeastern Peru around the Estacioń Biolo´gica date, group, species, sex, individual and time of Quebrada Blanco (EBQB, 4x21kS and 73x09kW), a defecation were recorded. After collection, the faecal field site located on the right bank of the Quebrada samples were immediately preserved in separate Blanco, a tributary of the Rio Tahuayo. The study 5.0 ml vials containing 10% buffered formalin (sol- area comprised y100 hectares of undisturbed pri- ution of 10% formaldehyde and sodium phosphate mary forest and contained a 100 mr100 m trail buffer, pH 7.0). Samples were stored at ambient system (for further details see Heymann, 1995). temperature. From each of the 43 individuals at least Additionally, samples were collected in and around 3 samples were collected on non-consecutive days. In the village Diamante on the opposite bank of the total, we have 356 faecal samples from the 8 study Quebrada Blanco. Diamante is the home of y40–50 groups. Additionally, faecal samples from 27 people people. The village centre of Diamante includes between the ages of 1 year and 66 years in Diamante 7 houses and a school. This population has no ad- were taken, at least 3 samples per individual from equate medical treatment for intestinal parasites. different days. In total, 85 human stool samples were The only other humans occurring in the area are collected. The finding of a parasite in any one of members of the scientific establishment with access multiple samples for a given individual resulted in a to anthelmintics. positive report of that parasite. To process the preserved faecal samples in the laboratory, a modified formalin-ethyl acetate sedi- Study animals mentation technique was used (Ash et al. 1994). The subjects of the study were 8 wild groups from Samples were microscopically examined for the 2 species of tamarins: 4 groups of moustached presence of eggs and larvae of different intestinal tamarins (Saguinus mystax mystax) and 4 groups of helminths. Eggs and larvae were identified by shape, saddleback tamarins (Saguinus fuscicollis nigrifrons). size and other visible structures as far as possible. Both species lived in mixed-species troops. Some of However, identification to species level was not the groups have been under observation for up to always possible based on microscopical examination 8 years (Mu¨ller, 2007). All group members are of eggs and larvae without the adult worms or known individually by natural markings (Lo¨ttker coprological cultures (Ash and Orihel, 1987; et al. 2004). The groups investigated differed in Gillespie et al. 2005). Measurements were made to their proximity to humans and their facilities. One of the nearest 0.1 mm¡S.D. using an ocular micrometer the mixed-species troops lived around the village fitted to a compound microscope.

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