Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-27T21:43:53.034Z Has data issue: false hasContentIssue false
  • English
  • Français

Intestinal parasites of endangered orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia

Published online by Cambridge University Press:  21 September 2009

E. M. LABES ,
D. HEGGLIN ,
F. GRIMM ,
W. NURCAHYO ,
M. E. HARRISON ,
M. L. BASTIAN  and
P. DEPLAZES
E. M. LABES*
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
D. HEGGLIN
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
F. GRIMM
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
W. NURCAHYO
Affiliation:
Gadjah Mada University, Faculty of Veterinary Medicine, Laboratory of Parasitology, 55281 Yogyakarta, Indonesia
M. E. HARRISON
Affiliation:
University of Cambridge, The Anatomy School, Wildlife Research Group, Downing Street, Cambridge CB2 3DY, UK University of Palangka Raya, Centre for the International Cooperation in Management of Tropical Peatlands, Palangka Raya, Central Kalimantan, Indonesia
M. L. BASTIAN
Affiliation:
Duke University, Department of Biological Anthropology and Anatomy, Science Drive, Box 90383, Durham, NC 27708-0383, USA
P. DEPLAZES
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
*
*Corresponding author: University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland. Tel: +41 (0)44 310 3210. Fax: +41 (0)44 310 3211. E-mail: elabes@bluewin.ch
Get access Rights & Permissions [Opens in a new window]

Summary

Faecal samples from 163 captive and semi-captive individuals, 61 samples from wild individuals and 38 samples from captive groups of Bornean orangutans (Pongo pygmaeus) in Kalimantan, Indonesia, were collected during one rainy season (November 2005–May 2006) and screened for intestinal parasites using sodium acetate-acetic acid-formalin-concentration (SAFC), sedimentation, flotation, McMaster- and Baermann techniques. We aimed to identify factors influencing infection risk for specific intestinal parasites in wild orangutans and individuals living in captivity. Various genera of Protozoa (including Entamoeba, Endolimax, Iodamoeba, Balantidium, Giardia and Blastocystis), nematodes (such as Strongyloides, Trichuris, Ascaris, Enterobius, Trichostrongylus and hookworms) and one trematode (a dicrocoeliid) were identified. For the first time, the cestode Hymenolepis was detected in orangutans. Highest prevalences were found for Strongyloides (individuals 37%; groups 58%), hookworms (41%; 58%), Balantidium (40%; 61%), Entamoeba coli (29%; 53%) and a trichostrongylid (13%; 32%). In re-introduction centres, infants were at higher risk of infection with Strongyloides than adults. Infection risk for hookworms was significantly higher in wild males compared with females. In groups, the centres themselves had a significant influence on the infection risk for Balantidium. Ranging patterns of wild orangutans, overcrowding in captivity and a shift of age composition in favour of immatures seemed to be the most likely factors leading to these results.

Keywords

Bornean orangutanPongo pygmaeusintestinal parasiteinfection risk parameter
Type
Research Article
Information
Parasitology , Volume 137 , Issue 1 , January 2010 , pp. 123 - 135
Copyright
Copyright © Cambridge University Press 2009

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

Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In Second International Symposium on Information Theory, Tsahkadsor, Armenian SSR (ed. Petrov, B. N. and Csaki, F.), pp. 267–281. Akademiai Kiado, Budapest, Hungary.Google Scholar
Anargyrou, K., Petrikkos, G. L., Suller, M. T. E., Skiada, A., Siakantaris, M. P., Osuntoyinbo, R. T., Pangalis, G. and Vaiopoulos, G. (2003). Pulmonary Balantidium coli infection in a leukemic patient. American Journal of Hematology 73, 180–183.CrossRefGoogle Scholar
Appelbee, A. J., Thompson, R. C. A. and Olson, M. E. (2005). Giardia and Cryptosporidium in mammalian wildlife – current status and future needs. Trends in Parasitology 21, 370–376.CrossRefGoogle ScholarPubMed
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.Google Scholar
Ashford, R. W., Reid, G. D. F. and Butynski, T. M. (1990). The intestinal faunas of man and mountain gorillas in a shared habitat. Annals of Tropical Medicine and Parasitology 84, 337–340.CrossRefGoogle Scholar
Bastian, M. L. (2008). Effects of a riverine dispersal barrier on cultural similarity in wild Bornean orangutans (Pongo pygmaeus wurmbii). Ph.D. dissertation, Duke University, Durham, NC, USA.Google Scholar
Brooks, J. I., Rud, E. W., Pilon, R. G., Smith, J. M., Switzer, W. M. and Sandstrom, P. A. (2002). Cross-species retroviral transmission from macaques to human beings. Lancet 260, 387–388.CrossRefGoogle Scholar
Burnham, K. and Anderson, D. (1998). Model Selection and Inference: A Practical Information-theoretic Approach. Springer, New York, USA.CrossRefGoogle Scholar
Chapman, C. A., Wasserman, M. D., Gillespie, T. R., Speirs, M. L., Lawes, M. J., Saj, T. L. and Ziegler, T. E. (2006). Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? American Journal of Physical Anthropology 131, 525–534.Google Scholar
Chen, F. C. and Li, W. H. (2001). Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. American Journal of Human Genetics 68, 444–456.CrossRefGoogle ScholarPubMed
Chitwood, M. (1970). Comparative relationships of some parasites of man and old and new world subhuman primates. Laboratory Animal Care 20, 389–394.Google Scholar
Collet, J. Y., Galdikas, B. M. F., Sugarjito, J. and Jojosudharmo, S. (1986). A coprological study of parasitism in orangutans (Pongo pygmaeus) in Indonesia. Journal of Medical Primatology 15, 121–129.CrossRefGoogle ScholarPubMed
Cross, J. H., Clarke, M. D., Cole, W. C., Lien, J. C., Partono, F., Djakaria, , Joesoef, A. and Oemijati, S. (1976). Parasitic infections in humans in West Kalimantan (Borneo), Indonesia. Tropical Geographical Medicine 28, 121–130.Google Scholar
Cross, J. H., Clarke, M. D., Durfee, P. T., Irving, G. S., Taylor, J., Partono, F., Joesoef, A., Hudojo, and Oemijati, S. (1975). Parasitology survey and seroepidemiology of amoebiasis in South Kalimantan (Borneo), Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 6, 52–60.Google ScholarPubMed
Cummins, L. B., Keeling, M. E. and McClure, H. M. (1973). Preventative medicine in anthropoids: parasite control. Laboratory Animal Science 23, 819–822.Google Scholar
Current, W. L. (1989). Cryptosporidiosis. In New Strategies in Parasitology (ed. McAdam, K. P. W. J.), pp. 257–273. Livingstone, Edinburgh, UK.Google Scholar
Delgado, R. A. and Van Schaik, C. P. (2000). The behavioural ecology and conservation of the orangutan (Pongo pygmaeus): A tale of two islands. Evolutionary Anthropology 9, 201–218.3.0.CO;2-Y>CrossRefGoogle Scholar
Djojosudharmo, S. and Gibson, A. T. (1993). Parasit intestinalis pada primat liar di Taman Nasional Gunung Leuser, Sumatra. In Simposium and Seminar Nasional Primata, Bandung, Sumatra. pp. 13–14.Google Scholar
Eberle, R. and Hilliard, J. K. (1989). Serological evidence for variation in the incidence of herpesvirus infections in different species of apes. Journal of Clinical Microbiology 27, 1357–1366.Google Scholar
Ezenwa, V. O. (2003). Habitat overlap and gastrointestinal parasitism in sympatric African bovids. Parasitology 126, 379–388.Google Scholar
Foitová, I., Huffman, M. A., Wisnu, N. and Olsansky, M. (2009). Parasites and their impacts on orangutan health. In Orangutans – Geographic Variation in Behavioral Ecology and Conservation (ed. Wich, S. A., Utami Atmoko, S. S., Setia, T. M. and Van Schaik, C. P.), pp. 157–169. Oxford University Press, Oxford, UK.Google Scholar
Freeland, W. J. (1980). Mangabey (Cercocebus albigena) movement patterns in relation to food availability and faecal contamination. Ecology 61, 1297–1303.Google Scholar
Freeman, A. S., Kinsella, J. M., Cipolletta, C., Deem, S. L. and Karesh, W. B. (2004). Endoparasites of Western Lowland Gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Journal of Wildlife Diseases 40, 775–781.CrossRefGoogle ScholarPubMed
Garber, P. A. (2008). Disease transmission from humans to wild apes: perspectives on the costs and benefits of research and conservation. American Journal of Primatology 70, 715.Google Scholar
Garcia, L. S. and Bruckner, D. A. (1997). Diagnostic Medical Parasitology, 3rd. edn.ASM Press, Washington, USA.Google Scholar
Graczyk, T. K., Bosco-Nizeyi, J., Ssebide, B., Thompson, R. C., Read, C. and Cranfield, M. R. (2002). Anthropozoonotic Giardia duodenalis genotype (assemblage) infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitolgy 88, 905–909.CrossRefGoogle ScholarPubMed
Graczyk, T. K., DaSilva, A. J., Cranfield, M. R., Nizeyi, J. B., Kalema, G. R. and Pieniazek, N. J. (2001). Cryptosporidium parvum genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitology Research 87, 368–370.Google Scholar
Graczyk, T. K., Lowenstine, L. J. and Cranfield, M. R. (1999). Capillaria hepatica (Nematoda) infections in human-habituated mountain gorillas (Gorilla gorilla beringei) of the Parc National de Volcans, Rwanda. Journal of Parasitology 85, 1168–1170.Google Scholar
Grimm, T. A., Beer, B. E., Hirsch, V. M. and Clouse, K. A. (2003). Simian immunodeficiency viruses from multiple lineages infect human macrophages: implications for cross-species transmission. Journal of Acquired Immune Deficiency Syndromes 32, 362–369.CrossRefGoogle ScholarPubMed
Groves, C. P. (1999). The taxonomy of orang-utans. In Orangutan Action Plan (ed. Yeager, C.), pp. 27–30. WWF, Jakarta, Indonesia.Google Scholar
Harper, J., Rice, J. M., London, W. T., Sly, D. L. and Middleton, C. (1982). Disseminated strongyloidosis in Erythrocebus patas. American Journal of Primatology 3, 89–98.CrossRefGoogle ScholarPubMed
Harrison, M. E. (2009). Orang-utan feeding behaviour in Sabangau, Central Kalimantan. Ph.D. dissertation, University of Cambridge, Cambridge, UK.Google Scholar
Hira, P. R. and Patel, B. G. (1980). Human strongyloidiasis due to the primate species Strongyloides fülleborni. Tropical and Geographical Medicine 32, 23–29.Google Scholar
Hope, K., Goldsmith, M. L. and Graczyk, T. (2004). Parasitic health of olive baboons in Bwindi Impenetrable National Park, Uganda. Veterinary Parasitology 122, 165–170.Google Scholar
Ho-Seong, C., Sung-Shik, S. and Nam-Yong, P. (2006). Balantidiasis in the gastric lymph nodes of Barbary sheep (Ammotragus lervia): an incidental finding. Journal of Veterinary Science 7, 207–209.Google Scholar
IUCN (2008). IUCN Red List of Threatened Species. www.redlist.orgGoogle Scholar
Johnson, J. B. and Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108.Google Scholar
Joseph, S. W., Carney, W. P., Van Peenen, P. F., Russell, D. and Saroso, J. S. (1978). Human parasitosis of the Malili area, South Sulawesi (Celebes) province, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 9, 264–271.Google Scholar
Karesh, W. B. and Reed, P. (2004). Population health concerns for lowland gorillas and other great apes. Diseases – the Third Major Threat for Wild Great Apes? Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 6–9 May, 2004.Google Scholar
Kaur, T., Singh, J., Tong, S., Humphrey, C., Clevenger, D., Tan, W., Szekely, B., Wang, Y., Li, Y., Muse, E. A., Kiyono, M., Hanamura, S., Inoue, E., Nakamura, M., Huffman, M. A., Jiang, B. and Nishida, T. (2008). Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. American Journal of Primatology 70, 738–744.Google Scholar
Kilbourn, A. M., Karesh, W. B., Wolfe, N. D., Bosi, E. J., Cook, R. A. and Andau, M. (2003). Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. Journal of Wildlife Diseases 39, 73–83.Google Scholar
Knott, C. D. (2001). Female reproductive ecology of the apes: implications for human evolution. In Reproductive Ecology and Human Evolution (ed. Ellison, P. T.), pp. 429–463. Walter de Gruyter, New York, USA.Google Scholar
Knott, C. D. (2005). Energetic responses to food availability in the great apes: Implications for hominin evolution. In Primate Seasonality: Implications for Human Evolution (ed. Brockman, D. and Van Schaik, C. P.), pp. 351–378. Cambridge University Press, Cambridge, UK.Google Scholar
Landsoud-Soukate, J., Tutin, C. E. G. and Fernandez, M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lopé Reserve, Gabon. Annals of Tropical Medicine and Parasitology 89, 73–79.Google Scholar
Leeflang, P. D. and Markham, R. J. (1986). Strongyloidosis in orang-utans (Pongo pygmaeus) at Perth Zoo: an apparently successful eradication programme. International Zoo Yearbook 24, 256–260. doi: 10.1111/J1748-1090.1985.TB02550-X.Google Scholar
Ley-Vela, M. (2005). Diurnal primate distribution and density in the Sabangau National Park, Central Kalimantan, Indonesia. M.Res. thesis, University of Roehampton, Roehampton, Surrey, UK.Google Scholar
Loehle, C. (1995). Social barriers to pathogen transmission in wild animal populations. Ecology 76, 326–335.Google Scholar
Maggioncalda, A. N., Sapolsky, R. M. and Czekala, N. M. (1999). Reproductive hormone profiles in captive male orangutans: Implications for understanding developmental arrest. American Journal of Physical Anthropology 109, 19–32.Google Scholar
Marti, H. and Escher, E. (1990). SAF – Eine alternative Fixierlösung für parasitologische Stuhluntersuchungen. Schweizerische Medizinische Wochenschrift 120, 1473–1476.Google Scholar
Michaud, C., Tantalean, M., Ique, C., Montoya, E. and Gozalo, A. (2003). A survey for helminth parasites in feral New World non-human primate populations and its comparison with parasitological data from man in the region. Journal of Medical Primatology 32, 341–45.CrossRefGoogle ScholarPubMed
Miyamoto, M. M., Koop, B. F., Slightom, J. L., Goodman, M. and Tennant, M. R. (1988). Molecular systematics of higher primates: Genealogical relations and classification. Proceedings of the National Academy of Sciences, USA 85, 7627–7631.Google Scholar
Mul, I. F., Paembonan, W., Singleton, I., Wich, S. A. and Van Bolhuis, E. G. (2007). Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology 28, 407–420. doi: 10.1007/S10764-007-9119-7.Google Scholar
Muller, R. (2002). Worms and Human Disease, 2nd edn.CABI Publishing, CABI International, Wallingford, UK.Google Scholar
Norusis, M. J. (1986). SPSS/PC+Advanced Statistics, 1st Edn.SPSS Inc., Chicago.Google Scholar
Nunn, C. L. and Altizer, S. (2006). Infectious Diseases in Primates. Behavior, Ecology and Evolution, 1st. Edn.Oxford University Press, Oxford, UK.Google Scholar
Ott-Joslin, J. E. (1993). Zoonotic diseases of nonhuman primates. In Zoo and Wild Animal Medicine: Current Therapy (ed. Fowler, M. E.), pp. 358–373. W. B. Saunders, Philadelphia, PA, USA.Google Scholar
Packer, C., Altizer, S., Appel, M., Brown, E., Martenson, J., O'Brian, S. J. and Roelke-Parker, M. (1999). Viruses of the Serengeti: patterns of infection and mortality in African lions. Journal of Animal Ecology 68, 1161–1178.Google Scholar
Pusey, A. E., Wilson, M. L. and Collins, D. A. (2008). Human Impacts, Disease Risk, and Population Dynamics in the Chimpanzees of Gombe National Park, Tanzania. American Journal of Primatology 70, 738–744.Google Scholar
Putrali, J., Carney, W. P., Stafford, E. E. and Tubo, S. (1977). Intestinal and blood parasites in the Banggai Kabupaten, Central Sulawesi, Indonesia. Southeast Southeast Asian Journal of Tropical Medicine and Public Health 8, 375–379.Google ScholarPubMed
Rijksen, H. D. (1978). A Field Study on Sumatran Orang Utans (Pongo pygmaeus abelli Lesson 1827): Ecology, Behaviour and Conservation. Ph.D. dissertation. Veenan, H. & Zonen B.V., Wageningen, The Netherlands.Google Scholar
Rijksen, H. D. and Meijaard, E. (1999). Our Vanishing Relative: the Status of Wild Orang-Utans at the Close of the Twentieth Century. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Schmidt, U. (1971). Parasitologische Kotuntersuchung durch ein neues Verduennungsverfahren. Tieraerztliche Umschau 26, 229–230.Google Scholar
Setia, T. M., Delgado, R. A., Utami Atmoko, S. S., Singleton, S. and Van Schaik, C. P. (2009). Social organizsation and male-female relationships. In Orangutans – Geographic Variation in Behavioral Ecology and Conservation (ed. Wich, S. A., Utami Atmoko, S. S., Setia, T. M. and Van Schaik, C. P.), pp. 245–253. Oxford University Press, Oxford, UK.Google Scholar
Singleton, I. and Van Schaik, C. P. (2001). Orangutan home range size and its determinants in a Sumatran swamp forest. International Journal of Primatology 22, 877–911.Google Scholar
Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. and Patton, S. (2000). Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. Journal of Zoo and Wildlife Medicine 31, 322–328.Google Scholar
Utami, S. S., Goossens, B., Bruford, M. W., De Ruiter, J. R. and Van Hooff, A. R. A. M. (2002). Male bimaturism and reproductive success in Sumatran orang-utans. Behavioral Ecology 13, 643–652.Google Scholar
Utami Atmoko, S. S., Singleton, I., Van Noordwijk, M. A., Van Schaik, C. P. and Mitra Setia, T. (2009 a). Male-male relationships in orangutans. In Orangutans – Geographic Variation in Behavioral Ecology and Conservation (ed. Wich, S. A., Utami Atmoko, S. S., Setia, T. M. and Van Schaik, C. P.), pp. 225–233. Oxford University Press, Oxford, UK.Google Scholar
Utami Atmoko, S. S., Mitra Setia, T., Goossens, B., James, S. S., Knott, C. D., Morrogh-Bernard, H. C., Van Schaik, C. P. and Van Noordwijk, M. A. (2009 b). Orangutan mating behaviour and strategies. In Orangutans – Geographic Variation in Behavioral Ecology and Conservation (ed. Wich, S. A., Utami Atmoko, S. S., Setia, T. M. and Van Schaik, C. P.), pp. 235–244. Oxford University Press, Oxford, UK.Google Scholar
Van Heuverswyn, F., Li, Y., Neel, C., Bailes, E., Keele, B. F., Liu, W., Loul, S., Butel, C., Liegeois, F., Bienvenue, Y., Ngolle, E. M., Sharp, P. M., Shaw, G. M., Delaporte, E., Hahn, B. H. and Peeters, M. (2006). Human immunodeficiency viruses: SIV infection in wild gorillas. Nature, London 444, 164.Google Scholar
Van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in orangutans. Primates 40, 69–86.Google Scholar
Van Schaik, C. P., Wich, S. A., Utami, S. S. and Odom, K. (2005). A simple alternative to line transects of nests for estimating orangutan densities. Primates 46, 249–254.Google Scholar
Viney, M. E. and Lok, J. B. (2007). Strongyloides spp. In The C. elegans Research Community, WormBook (ed. Hodgkin, J. and Anderson, P.), www.wormbook.org. doi/10.1895/wormbook.1.141.Google Scholar
Vitone, N. D., Altizer, S. M. and Nunn, C. L. (2004). Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolutionary Ecology Research 6, 1–17.Google Scholar
Warren, K. S. (2001). Orangutan conservation – epidemiological aspects of health management and population genetics. Ph.D. dissertation, Murdoch University, Australia.Google Scholar
Wells, S. K., Sargeant, E., Andrews, M. E. and Anderson, D. E. (1990). Gastrointestinal disorders. In Medical Management of the Orangutan (ed. Wells, S.), pp. 65–66. The Audobon Institute, Louisiana, USA.Google Scholar
Whitfield, J. (2003). Ape populations decimated by hunting and Ebola virus. Nature, London 422, 551.Google Scholar
Wich, S. A., Meijaard, E., Marshall, A. J., Husson, S., Ancrenaz, M., Lacy, R. C., Van Schaik, C. P., Sugardjito, J., Simorangkir, T., Traylor-Holzer, K., Doughty, M., Supriatna, J., Dennis, R., Gumal, M., Knott, C. D. and Singleton, I. (2008). Distribution and conservation status of the orangutan (Pongo spp.) on Borneo and Sumatra: how many remain? Oryx 42, 329–339.Google Scholar
Wich, S. A., Sterck, E. H. M. and Utami, S. S. (1999). Are orangutan females as solitary as chimpanzee females? Folia Primatologia 70, 23–28.Google Scholar
Williams, J. M., Lonsdorf, E. V., Wilson, M. L., Schumacher-Stankey, J., Goodall, J. and Pusey, A. E. (2008). Causes of death in the Kasekela chimpanzees of Gombe National Park, Tanzania. American Journal of Primatology 70, 738–744.Google Scholar
Xu, X. and Arnason, U. (1996). The mitochondrial DNA molecule of Sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan. Journal of Molecular Evolution 43, 431–437.CrossRefGoogle Scholar
Yamagiwa, J. (2004). Diet and foraging of the great apes: ecological constraints on their social organizations and implications for their divergence. In The Evolution of Thought: Evolutionary Origins of Great Ape Intelligence (ed. Russon, A. E. and Begun, D. R.), pp. 210–233. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar