Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-18T12:05:49.490Z Has data issue: false hasContentIssue false
  • English
  • Français

Human contact influences the foraging behaviour and parasite community in long-tailed macaques

Published online by Cambridge University Press:  30 January 2013

ALEXANDRA WENZ-MÜCKE ,
PAIBOON SITHITHAWORN ,
TREVOR N. PETNEY  and
HORST TARASCHEWSKI
ALEXANDRA WENZ-MÜCKE*
Affiliation:
KIT, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
PAIBOON SITHITHAWORN
Affiliation:
University of Khon Kaen, Faculty of Medicine, Department of Parasitology, 40002 Khon Kaen, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
TREVOR N. PETNEY
Affiliation:
KIT, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
HORST TARASCHEWSKI
Affiliation:
KIT, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
*
*Corresponding author: KIT, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany. Tel: +49 721 60842701. Fax: +49 721 6087655. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

Human–wildlife interactions have reached unprecedented levels, and humans are influencing the earth's ecosystems more rapidly and extensively than ever before. This situation is cause for serious concern, especially since disease interactions between wildlife and humans have been recognized as major conservation threats. In this study, long-tailed macaques, Macaca fascicularis, from 2 forest parks located in north-eastern Thailand were investigated to determine the influence of habitat modification by humans on helminth parasite associations in non-human primates. Macaque populations with contact to anthropogenically modified environments were compared with sylvatic groups in nearby natural environments. In order to test for human–non-human primate transmission of parasites, the local human populations were also examined. Humans were infected with a number of potentially pathogenic parasites, including Opisthorchis viverrini and Strongyloides stercoralis. However, eggs of these helminths were not detected in macaque feces. Thus, no direct parasite transfer from humans to non-human primates could be confirmed. However, macaque groups with more frequent contact with human-modified habitats, and a higher portion of human-provided food in their diet, had significantly higher prevalences and intensities of Strongyloides fuelleborni and of an intestinal fluke (probably Haplorchis sp.) than sylvatic groups. Positive correlations were found between the time foraging on the ground and infection with S. fuelleborni, and the amount of human-provided food and intestinal fluke infection. Human alteration of habitat and associated modifications in non-human primate behaviour are likely to play a role in determining the occurrence, prevalence and intensity of zoonotic helminth infection of wild non-human primates.

Keywords

primatesmacaquesparasiteshelminth infectionhumansbehaviourhabitat alteration
Type
Research Article
Information
Parasitology , Volume 140 , Issue 6 , May 2013 , pp. 709 - 718
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altman, J. and Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-foraging baboons. American Journal of Primatology 15, 213–221.CrossRefGoogle Scholar
Ash, L. R. and Orihel, T. C. (1987). Parasites: a Guide to Laboratory Procedures and Identification. American Society of Clinical Pathologists Press, Chicago, IL, USA.Google Scholar
Ash, L. R., Orihel, T. C. and Savioli, L. (1994). Bench Aids for the Diagnosis of Intestinal Parasites. World Health Organization, Geneva, Switzerland.Google Scholar
Box, H. O. (1991). Training for life after release: simian primates as examples. Symposia of the Zoological Society of London 62, 111–123.Google Scholar
Chapman, C. A., Gillespie, T. R. and Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology 14, 134–144. doi: 10.1002/evan.20068.CrossRefGoogle Scholar
Chapman, C. A. and Peres, C. A. (2001). Primate conservation in the new millennium: the role of scientists. Evolutionary Anthropology 10, 16–33.3.0.CO;2-O>CrossRefGoogle Scholar
Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T. and Austad, K. M. (2006). Life on the edge: the gastrointestinal parasite from forest edge and interior primate groups. American Journal of Primatology 68, 1–12. doi: 10.1002/ajp.20233.CrossRefGoogle ScholarPubMed
Charlwood, J. D. and Alecrim, W. A. (1989). Capture-recapture studies with the South American malaria vector Anopheles darlingi, Root. Annals of Tropical Medicine and Parasitology 83, 569–576.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. and Savioli, L. (2006). Handbook of Helminthiasis for Public Health. CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle ScholarPubMed
Dobson, A. P. and May, R. M. (1986). Disease and conservation. In Conservation Biology: The Science of Scarcity and Diversity (ed. Soule, M. and Sunderland, M. A.), pp. 345–365. Sinauer Associates Inc., Sunderland, MA, USA.Google Scholar
Eley, R. M., Strum, S. C., Muchemi, G. and Reid, G. D. F. (1989). Nutrition, body condition, activity patterns and parasitism of free-ranging baboons (Papio anubis) in Kenya. American Journal of Primatology 18, 209–219. doi: 10.1002/ajp.1350180304.CrossRefGoogle ScholarPubMed
Else, J. G. and Lee, P. C. (1986). Primate–human conflict. In Primate Ecology and Conservation. (ed. Else, J. G. and Lee, P. C.), pp. 213–214. Cambridge University Press, Cambridge, UK.Google Scholar
Engels, D., Sinzinkayo, E. and Gryseels, B. (1996). Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. American Journal of Tropical Medicine and Hygiene 54, 319–324.CrossRefGoogle ScholarPubMed
Engels, D., Sinzinkayo, E., DeVlas, S. J. and Gryseels, B. (1997). Intraspecimen fecal egg count variation in Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 57, 571–577.CrossRefGoogle ScholarPubMed
Esch, G. W. and Fernandez, J. C. (1993). A Functional Biology of Parasitism: Ecological and Evolutionary Implications. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Flynn, R. J. (1973). Parasites of Laboratory Animals. Iowa State University Press, Ames, IA, USA.Google Scholar
Foley, J. A., DeFries, R., Asner, G. P., Barford, C., Bonan, G., Carpenter, S. R., Chapin, F. S., Coe, M. T., Daily, G. C., Gibbs, H. K., Helkowski, J. H., Holloway, T., Howard, E. A., Kucharik, C. J., Monfreda, C., Patz, J. A., Prentice, I. C., Ramankutty, N. and Snyder, P. K. (2002). Global consequences of land use. Science 309, 570–574. doi: 10.1126/science.111772.CrossRefGoogle Scholar
Fried, B., Graczyk, T. K. and Tamang, L. (2004). Food-borne intestinal trematodiases in humans. Parasitology Research 93, 159–170.CrossRefGoogle ScholarPubMed
Fuentes, A. (2006). Human culture and monkey behaviour; assessing the contexts of potential pathogen transmission between macaques and humans. American Journal of Primatology 68, 880–896. doi: 10.1002/ajp.20295.CrossRefGoogle ScholarPubMed
Gillespie, T. R. and Chapman, C. A. (2006). Forest fragment attributes predict parasite infection dynamics in primate metapopulations. Conservation Biology 20, 441–448.CrossRefGoogle ScholarPubMed
Gillespie, T. R., Greiner, E. C. and Chapman, C. A. (2005). Gastrointestinal parasites of the colobus monkeys of Uganda. Journal of Parasitology 91, 569–573.CrossRefGoogle ScholarPubMed
Gillespie, T. R., Lonsdorf, E. V., Canfield, E. P., Meyer, D. J., Nadler, Y., Raphael, J., Pusey, A. E., Pond, J., Pauley, J., Mlengeya, T. and Travis, D. A. (2010). Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. American Journal of Physical Anthropology. 143, 534–544.CrossRefGoogle ScholarPubMed
Grove, D. I. (1996). Human strongyloidiasis. Advances in Parasitology 38, 251–309.CrossRefGoogle ScholarPubMed
Hochachka, W. M. and Dhondt, A. A. (2000). Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Sciences, USA 97, 303–530. doi: 10.1073/pnas.080551197.CrossRefGoogle ScholarPubMed
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258. doi: 10.1126/science.282.5397.2256.CrossRefGoogle ScholarPubMed
Hudson, P. J., Rizzoli, A. P., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. (2002). The Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
IUCN (2011). IUCN Red List of Threatened Species. Version 2011.2 www.iucnredlist.orgGoogle Scholar
Keet, D. F., Krick, N. P. J., Bengis, R. G., Grobler, D. G. and Michel, A. (2000). The rise and fall of tuberculosis in a free-ranging chacma baboon troop in the Kruger National Park. Onderstepoort Journal of Veterinary Research 67, 115–122.Google Scholar
Keymer, A. E. and Hiorns, R. W. (1986). Faecal egg counts and nematode fecundity: Heligmosomoides polygyrus and laboratory mice. Parasitology 93, 189–203.CrossRefGoogle ScholarPubMed
Koga, K., Kasuya, S., Khamboonruang, C., Sukhavat, K., Ieda, M., Takatsuka, N., Kita, K. and Ohtomo, H. (1991). A modified agar plate method for detection of Strongyloides stercoralis. American Journal of Tropical Medicine and Hygiene 45, 518–521.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2003). Is disease increasing or decreasing, and does it impact or maintain biodiversity? Journal of Parasitology 89, 5101–5105.Google Scholar
Laurenson, K., Sillero-Zubiri, C., Thompson, H., Shiferaw, F., Thirgood, S. and Malcolm, J. (1998). Disease as a threat to endangered species: Ethiopian wolves, domestic dogs and canine pathogens. Animal Conservation 1, 273–280.CrossRefGoogle Scholar
Legesse, M. and Erko, B. (2004). Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethopis (vervet) from four localities in Ethiopia. Acta Tropica 90, 231–236.CrossRefGoogle ScholarPubMed
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555–573.CrossRefGoogle Scholar
Lyles, A. M. and Dobson, A. P. (1993). Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine 24, 315–326.Google Scholar
MAFF (1979). Parasitological Laboratory Techniques, Technical Bulletin No. 18. Ministry of Agriculture, Fisheries and Food Manual of Veterinary, Her Majestey's Stationery Office, London, UK.Google Scholar
Marques, A. C. (1987). Human migration and the spread of malaria in Brazil. Parasitology Today 3, 166–170.CrossRefGoogle Scholar
Martin, P. and Bateson, P. (1993). Measuring Behaviour: An Introductory Guide, 2nd Edn.Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
May, R. M. (1988). Conservation and disease. Conservation Biology 2, 28–30.CrossRefGoogle Scholar
Nunn, C., Gittleman, J. L. and Antonovics, J. (2000). Promiscuity and the primate immune system. Science 290, 1168–1170. doi: 10.1126/science.290.5494.1168CrossRefGoogle ScholarPubMed
Ooi, H. K., Tenora, F., Itoh, K. and Kamiya, M. (1993). Comparative study of Trichuris trichiura from nonhuman primates and from man, and their differences with T. suis. Journal of Veterinary Medical Science 55, 363–366.CrossRefGoogle ScholarPubMed
Patz, J. A., Daszak, P., Tabor, G. M., Aguirre, A. A., Pearl, M., Epstein, J., Wolfe, N. D., Kilpatrick, M. A., Foufopoulos, J., Molyneux, D. and Bradley, D. J. (2004). Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112, 1092–1098. doi:10.1289/ehp.6877.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Quinnell, R. J., Slater, A. F., McKean, P. G. and Dale, D. D. S. (1990). Epidemiology and immunology of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory-secretory and cuticular collagen antigens. Parasitology 100, 317–326.CrossRefGoogle Scholar
Pungpak, S., Radomyos, P., Radomyos, B., Schelp, F. P., Jongsuksuntigul, P. and Bunnag, D. (1998). Treatment of Opisthorchis viverrini and intestinal fluke infections with praziquentel. Southeast Asian Journal of Tropical Medicine and Public Health 29, 246–249.Google Scholar
Radomyos, B., Wongsaroj, T., Wilairatana, P., Radomyos, P., Praevanich, R., Meesomboon, V. and Jongsuksuntikul, P. (1998). Opisthorchiasis and intestinal fluke infections in northern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 29, 123–127.Google ScholarPubMed
Remfry, J. (1978). The incidence, pathogenesis and treatment of helminth infections in rhesus monkeys (Macaca mulatta). Laboratory Animals 12, 213–218.CrossRefGoogle ScholarPubMed
Rolland, R. M., Hausfater, G., Marshall, B. and Levy, S. B. (1985). Antibiotic-resistant bacteria in wild primates – increased prevalence in baboons feeding on human refuse. Applied Environmental Microbiology 49, 791–794.CrossRefGoogle ScholarPubMed
Ross, A. G. P., Li, Y., Sleigh, A. C., Williams, G. M. and McManus, D. P. (1998). Faecal egg aggregation in humans infected with Schistosoma japonicum in China. Acta Tropica 70, 205–210. doi: http://dx.doi.org/10.1016/S0001-706X(98)00022-9.CrossRefGoogle ScholarPubMed
Routman, E., Miller, R. D., Phillips-Conroy, J. and Hartl, D. L. (1985). Antibiotic resistance and population structure in Escherichia coli from free-ranging African yellow baboons. Applied Environmental Microbiology 50, 749–754.CrossRefGoogle ScholarPubMed
Sapolsky, R. M. and Else, J. G. (1987). Bovine tuberculosis in a wild baboon population: epidemiological aspects. Journal of Medical Primatology 16, 229–235.CrossRefGoogle Scholar
Sithithaworn, P., Tesana, S., Pipitgool, V., Kaewkes, S., Pairojkul, C., Sripa, B., Pauparoj, A. and Thaiklar, A. (1991). Relationship between faecal egg count and worm burden of Opisthorchis viverrini in human autopsy cases. Parasitology 103, 277–281. doi: http://dx.doi.org/10.1017/S0031182000062594.CrossRefGoogle Scholar
Smith, K. F., Sax, D. F. and Lafferty, K. D. (2006). Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20, 1349–1357. doi: 10.1111/j.1523-1739.2006.00524.x.CrossRefGoogle ScholarPubMed
Srisawangwong, T., Sithithaworn, P. and Tesana, S. (1997). Metacercariae isolated from cyprinoid fish in Khon Kaen district by digestion technique. Southeast Asian Journal of Tropical Medicine and Public Health 28, 224–226.Google Scholar
Standley, C. J., Mugisha, L., Verweij, J. J., Adriko, M., Arinaitwe, M., Rowell, C., Atuhaire, A., Betson, M., Hobbs, E., van Tulleken, C. R., Kane, R. A., van Lieshout, L., Ajarova, L., Kabatereine, N. B. and Stothard, J. R. (2011). Confirmed infection with intestinal schistosomiasis in semi-captive wild-born chimpanzees on Ngambe Island, Uganda. Vector-Borne and Zoonotic Diseases 11, 169–176.CrossRefGoogle Scholar
Standley, C. J., Mugisha, L., Dobson, A. P. and Stothard, J. R. (2012). Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa. Journal of Helminthology 86, 131–140.CrossRefGoogle ScholarPubMed
Stuart, M. D. and Strier, K. B. (1995). Primates and parasites: a case for a multidisciplinary approach. International Journal of Primatology 15, 577–593. doi: 10.1007/BF02735282.CrossRefGoogle Scholar
Sukontason, K., Piangjai, S., Muangyimpong, Y., Sukontason, K., Methanitikorn, R. and Chaithong, U. (1999). Prevalence of trematode metacercariae in cyprinoid fish of Ban Pao district, Chiang Mai province, northern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 30, 365–370.Google Scholar
Sukontason, K., Upunyo, P., Sukontason, K. L. and Piangjai, S. (2005). Evidence of Haplorchis taichui infection as a pathogenic parasite: three case reports. Scandinavian Journal of Infectious Diseases 37, 388–390. doi: 10.1080/00365540510034473CrossRefGoogle ScholarPubMed
Taraschewski, H. (2006). Hosts and parasites as aliens. Journal of Helminthology 80, 99–128. doi: 10.1079/JOH2006364.CrossRefGoogle ScholarPubMed
Viney, M., Ashford, R. W. and Barnish, G. (1991). A taxonomic study of Strongyloides Grassi, 1879 (Nematoda) with special reference for Strongyloides fuelleborni von Linstow, 1905 in man in Papua New Guinea and the description of a new subspecies. Systematic Parasitology 18, 95–109.CrossRefGoogle Scholar
Wenz, A., Heymann, E. W., Petney, T. and Taraschewski, H. (2010). The influence of human settlements on the parasite community in two species of Peruvian tamarin. Parasitology 137, 675–684. doi: http://dx.doi.org/10.1017/S0031182009991570.CrossRefGoogle ScholarPubMed
Weyher, A. H., Ross, C. and Semple, S. (2006). Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. International Journal of Primatology 27, 2519–1534. doi: 10.1007/s10764-006-9089-1.CrossRefGoogle Scholar
World Health Organization (2006). Preventive Chemotherapy in Human Helminthiasis: Coordinated Use of Antihelminthic Drugs in Control Interventions: a Manual for Health Professionals and Programme Managers. World Health Organization, Geneva, Switzerland.Google Scholar
Wolfe, N. D., Eifel, M. N., Gockowski, J., Muchaal, P. K., Nolte, C., Proser, A. Tassey, Torimiro, J. Ndongo, Weise, S. F. and Burke, D. S. (2000). Deforestation, hunting and the ecology of microbial emergence. Global Change and Human Health 1, 10–25.CrossRefGoogle Scholar
Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourne, A., Spielman, A. and Lal, A. A. (1998). Wild primate populations in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4, 149–158.CrossRefGoogle ScholarPubMed
Wolfe, N. D., Prosser, A. Tassey, Carr, J. K., Tamoufe, U., Mpoudi-Ngole, E., Torimiro, J. Ndongo, LeBreton, M., McCutchan, F. E., Birx, D. L. and Burke, D. S. (2004). Exposure to nonhuman primates in rural Cameroon. Emerging Infectious Diseases 10, 2094–2099.CrossRefGoogle ScholarPubMed
Woodford, M. H., Butynski, T. M. and Karesh, W. B. (2002). Habituating the great apes: the disease risks. Oryx 36, 153–160. doi: 10.1017/S0030605302000224.CrossRefGoogle Scholar
Wykoff, D. E. (1964). Studies on Opisthorchis viverrini in Thailand. Experimental Laboratory Hosts. Annual Progress Report. http://www.afrims.org/weblib/eapr/1963/APR63p161-164.pdfGoogle Scholar
Yamashita, J. (1963). Ecological relationship between parasites and primates. Primates 4, 1–96. doi: 10.1007/BF01659699.CrossRefGoogle Scholar