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

Parasitology

Volumn 137, Issue 1, 2010, Pages 123-135

  Labes, E M ^a   Hegglin, D ^a   Grimm, F ^a   Nurcahyo, W ^b   Harrison, M E ^c,d   Bastian, M L ^e   Deplazes, P ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b GADJAH MADA UNIVERSITY   (Indonesia)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF PALANGKA RAYA   (Indonesia)

^e DUKE UNIVERSITY   (United States)

Author keywords

Bornean orangutan; Infection risk parameter; Intestinal parasite; Pongo pygmaeus

Indexed keywords

ARTICLE; BORNEO; CESTODE; ENDANGERED SPECIES; FEMALE; HOOKWORM; INDONESIA; INFECTION RISK; INTESTINE PARASITE; MALE; MULTIVARIATE LOGISTIC REGRESSION ANALYSIS; NEMATODE; NONHUMAN; ORANG UTAN; PARASITE PREVALENCE; PRIORITY JOURNAL; PROTOZOON; SEX DIFFERENCE; TREMATODE;

ANIMALS; ANIMALS, WILD; ANIMALS, ZOO; APE DISEASES; BORNEO; ENDANGERED SPECIES; FECES; FEMALE; HELMINTHIASIS, ANIMAL; INTESTINAL DISEASES, PARASITIC; LOGISTIC MODELS; MALE; ODDS RATIO; PONGO PYGMAEUS; PREVALENCE; PROTOZOAN INFECTIONS, ANIMAL;

ANCYLOSTOMATOIDEA; ASCARIS; BALANTIDIUM; BLASTOCYSTIS; CESTODA; DICROCOELIIDAE; ENDOLIMAX; ENTAMOEBA; ENTAMOEBA COLI; ENTEROBIUS; GIARDIA; HYMENOLEPIS (CESTODA); IODAMOEBA; NEMATODA; PONGO PYGMAEUS; PONGO PYGMAEUS PYGMAEUS; PROTOZOA; STRONGYLOIDES; TREMATODA; TRICHOSTRONGYLIDAE; TRICHOSTRONGYLUS; TRICHURIS;

EID: 75149146436     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182009991120     Document Type: Article

References (81)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. Burnham, K. and Anderson, D. (1998). Model Selection and Inference: A Practical Information-theoretic Approach. Springer, New York, USA.
9. 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.
10. 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.
11. Chitwood, M. (1970). Comparative relationships of some parasites of man and old and new world subhuman primates. Laboratory Animal Care 20, 389-394.
12. 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.
13. 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.
14. 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.
15. Cummins, L. B., Keeling, M. E. and McClure, H. M. (1973). Preventative medicine in anthropoids: parasite control. Laboratory Animal Science 23, 819-822.
16. Current, W. L. (1989). Cryptosporidiosis. In New Strategies in Parasitology (ed. McAdam, K. P. W. J.), pp. 257-273. Livingstone, Edinburgh, UK.
17. 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.
18. 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.
19. 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.
20. Ezenwa, V. O. (2003). Habitat overlap and gastrointestinal parasitism in sympatric African bovids. Parasitology 126, 379-388.
21. 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.
22. Freeland, W. J. (1980). Mangabey (Cercocebus albigena) movement patterns in relation to food availability and faecal contamination. Ecology 61, 1297-1303.
23. 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.
24. 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.
25. Garcia, L. S. and Bruckner, D. A. (1997). Diagnostic Medical Parasitology, 3rd. edn. ASM Press, Washington, USA.
26. 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.
27. 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.
28. 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.
29. 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.
30. Groves, C. P. (1999). The taxonomy of orang-utans. In Orangutan Action Plan (ed. Yeager, C.), pp. 27-30. WWF, Jakarta, Indonesia.
31. 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.
32. Harrison, M. E. (2009). Orang-utan feeding behaviour in Sabangau, Central Kalimantan. Ph.D. dissertation, University of Cambridge, Cambridge, UK.
33. Hira, P. R. and Patel, B. G. (1980). Human strongyloidiasis due to the primate species Strongyloides fülleborni. Tropical and Geographical Medicine 32, 23-29.
34. 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.
35. 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.
36. IUCN (2008). IUCN Red List of Threatened Species. www.redlist.org
37. Johnson, J. B. and Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101-108.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. Loehle, C. (1995). Social barriers to pathogen transmission in wild animal populations. Ecology 76, 326-335.
48. 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.
49. Marti, H. and Escher, E. (1990). SAF - Eine alternative Fixierlösung fü r parasitologische Stuhluntersuchungen. Schweizerische Medizinische Wochenschrift 120, 1473-1476.
50. 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, 341-345
51. 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.
52. 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. (Pubitemid 46944819)
53. Muller, R. (2002). Worms and Human Disease, 2nd edn. CABI Publishing, CABI International, Wallingford, UK.
54. Norusis, M. J. (1986). SPSS/PC+Advanced Statistics, 1st Edn. SPSS Inc., Chicago.
55. Nunn, C. L. and Altizer, S. (2006). Infectious Diseases in Primates. Behavior, Ecology and Evolution, 1st. Edn. Oxford University Press, Oxford, UK.
56. 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.
57. 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.
58. 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.
59. 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. (Pubitemid 8269057)
60. 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.
61. 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.
62. Schmidt, U. (1971). Parasitologische Kotuntersuchung durch ein neues Verduennungsverfahren. Tieraerztliche Umschau 26, 229-230.
63. 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.
64. 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.
65. 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.
66. 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.
67. Utami Atmoko, S. S., Singleton, I., Van Noordwijk, M. A., Van Schaik, C. P. and Mitra Setia, T. (2009a). 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.
68. 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. (2009b). 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.
69. 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.
70. Van Schaik, C. P. (1999). The socioecology of fissionfusion sociality in orangutans. Primates 40, 69-86.
71. 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.
72. 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.
73. 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.
74. Warren, K. S. (2001). Orangutan conservation - epidemiological aspects of health management and population genetics. Ph.D. dissertation, Murdoch University, Australia.
75. 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.
76. Whitfield, J. (2003). Ape populations decimated by hunting and Ebola virus. Nature, London 422, 551.
77. 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.
78. 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.
79. 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.
80. 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.
81. 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.