Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo
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 f...
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doaj-a9d6bba6d5f64bb89c42881fd5c823412020-11-24T23:15:14ZengElsevierInternational Journal for Parasitology: Parasites and Wildlife2213-22442017-12-0163320329Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in BorneoAnnette Klaus0Elke Zimmermann1Kathrin Monika Röper2Ute Radespiel3Senthilvel Nathan4Benoit Goossens5Christina Strube6Institute for Parasitology, University of Veterinary Medicine Hannover, Hannover, Buenteweg 17, 30559 Hannover, Germany; Institute of Zoology, University of Veterinary Medicine Hannover, Hannover, Buenteweg 17, 30559 Hannover, GermanyInstitute of Zoology, University of Veterinary Medicine Hannover, Hannover, Buenteweg 17, 30559 Hannover, GermanyInstitute of Zoology, University of Veterinary Medicine Hannover, Hannover, Buenteweg 17, 30559 Hannover, GermanyInstitute of Zoology, University of Veterinary Medicine Hannover, Hannover, Buenteweg 17, 30559 Hannover, GermanySabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, 88100 Kota Kinabalu, Sabah, MalaysiaSabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, 88100 Kota Kinabalu, Sabah, Malaysia; Organisms and Environment Division, School of Biosciences, Cardiff University, The Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, United Kingdom; Danau Girang Field Centre, C/o Sabah Wildlife Department, Kota Kinabalu, Sabah, Malaysia; Sustainable Places Research Institute, Cardiff University, 33 Park Pl, Cardiff CF10 3BA, United KingdomInstitute for Parasitology, University of Veterinary Medicine Hannover, Hannover, Buenteweg 17, 30559 Hannover, Germany; Corresponding author.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. Keywords: Nasalis larvatus, Gastrointestinal parasites, Co-infection, Conservation, South-East Asia, Malaysia, Zoonosishttp://www.sciencedirect.com/science/article/pii/S2213224417300238 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Annette Klaus Elke Zimmermann Kathrin Monika Röper Ute Radespiel Senthilvel Nathan Benoit Goossens Christina Strube |
spellingShingle |
Annette Klaus Elke Zimmermann Kathrin Monika Röper Ute Radespiel Senthilvel Nathan Benoit Goossens Christina Strube Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo International Journal for Parasitology: Parasites and Wildlife |
author_facet |
Annette Klaus Elke Zimmermann Kathrin Monika Röper Ute Radespiel Senthilvel Nathan Benoit Goossens Christina Strube |
author_sort |
Annette Klaus |
title |
Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo |
title_short |
Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo |
title_full |
Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo |
title_fullStr |
Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo |
title_full_unstemmed |
Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo |
title_sort |
co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, nasalis larvatus) in borneo |
publisher |
Elsevier |
series |
International Journal for Parasitology: Parasites and Wildlife |
issn |
2213-2244 |
publishDate |
2017-12-01 |
description |
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. Keywords: Nasalis larvatus, Gastrointestinal parasites, Co-infection, Conservation, South-East Asia, Malaysia, Zoonosis |
url |
http://www.sciencedirect.com/science/article/pii/S2213224417300238 |
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