Understanding determinants shaping infection risk of endangered wildlife is a major topic in conservation medicine. The proboscis monkey, Nasalis larvatus, an endemic primate flagship species for conservation in Borneo, is endangered through habitat loss, but can still be found in riparian lowland and mangrove forests, and in some protected areas. To assess socioecological and anthropogenic influence on intestinal helminth infections in N. larvatus, 724 fecal samples of harem and bachelor groups, varying in size and the number of juveniles, were collected between June and October 2012 from two study sites in Malaysian Borneo: 634 samples were obtained from groups inhabiting the Lower Kinabatangan Wildlife Sanctuary (LKWS), 90 samples were collected from groups of the Labuk Bay Proboscis Monkey Sanctuary (LBPMS), where monkeys are fed on stationary feeding platforms. Parasite risk was quantified by intestinal helminth prevalence, host parasite species richness (PSR), and eggs per gram feces (epg). Generalized linear mixed effect models were applied to explore whether study site, group type, group size, the number of juveniles per group, and sampling month predict parasite risk. At the LBPMS, prevalence and epg of Trichuris spp., strongylids, and Strongyloides spp. but not Ascaris spp., as well as host PSR were significantly elevated. Only for Strongyloides spp., prevalence showed significant changes between months; at both sites, the beginning rainy season with increased precipitation was linked to higher prevalence, suggesting the external life cycle of Strongyloides spp. to benefit from humidity. Higher prevalence, epgs, and PSR within the LBPMS suggest that anthropogenic factors shape host infection risk more than socioecological factors, most likely via higher re-infection rates and chronic stress. Noninvasive measurement of fecal parasite stages is an important tool for assessing transmission dynamics and infection risks for endangered tropical wildlife. Findings will contribute to healthcare management in nature and in anthropogenically managed environments.
Non-human primates of South-East Asia remain under-studied concerning parasite epidemiology and co-infection patterns. Simultaneously, efforts in conservation demand knowledge of parasite abundance and biodiversity in threatened species. The Endangered proboscis monkey, Nasalis larvatus, a primate flagship species for conservation in Borneo, was investigated in the present study. Habitat loss and fragmentation are among the greatest threats to bachelor and harem groups of this folivorous colobine. Designed as a follow-up study, prevalence and co-infection status of intestinal parasites from N. larvatus in a protected area in Malaysian Borneo were analyzed from fecal samples using a flotation method. For the first time, the intestinal parasite co-infection patterns were examined using quantitative analyses. Overall, 92.3% of fecal samples (N = 652) were positive for helminth eggs. Five helminth groups were detected: (1) trichurids (82.7% prevalence) including Trichuris spp. (82.1%) and Anatrichosoma spp. (1.4%), (2) strongyles (58.9%) including Trichostrongylus spp. (48.5%) and Oesophagostomum/Ternidens spp. (22.8%), (3) Strongyloides fuelleborni (32.7%), (4) Ascaris lumbricoides (8.6%), and (5) Enterobius spp. (5.5%). On average, an individual was co-infected with two different groups. Significant positive associations were found for co-infections of trichurids with strongyles and S. fuelleborni as well as S. fuelleborni with A. lumbricoides and strongyles. This study shows a high prevalence of various gastrointestinal helminths with potential transmission pathways primarily related to soil and with zoonotic relevance in wild proboscis monkeys in their remaining natural habitats. Observed positive associations of trichurids with strongyles and Strongyloides spp. may result from the high prevalence of trichurids. Similarly, positive associations between Strongyloides and Ascaris were found, both of which typically occur predominantly in juvenile hosts. These findings should be considered when proposing conservation actions in altered habitats nearby human settlements and when managing captive populations.