International Journal of Primatology

, Volume 35, Issue 2, pp 463–475 | Cite as

Gastrointestinal Parasites of Savanna Chimpanzees (Pan troglodytes schweinfurthii) in Ugalla, Tanzania

  • Barbora Kalousová
  • Alexander K. Piel
  • Kateřina Pomajbíková
  • David Modrý
  • Fiona A. Stewart
  • Klára J. Petrželková
Article

Abstract

Understanding variability in patterns of parasite infections requires studies of multiple populations inhabiting a variety of habitats. Gastrointestinal parasites of chimpanzees (Pan troglodytes) have been studied extensively at several forested sites, but the parasite fauna of chimpanzees living in dry, open habitats is less well known. We studied the parasites of savanna chimpanzees (Pan troglodytes schweinfurthii) living in the Issa Valley, Ugalla (Tanzania). We examined 119 fresh fecal samples using standard coproscopical methods. We detected protozoans including Blastocystis sp., Entamoeba coli, E. histolytica/dispar, Iodamoeba buetschlii, Troglodytella abrassarti, and Troglocorys cava, but only two types of spirurid nematodes among the helminths. The parasites of the Ugalla chimpanzees differ from those of forest chimpanzees in the absence of Strongyloides sp. and strongylid nematodes and a high prevalence of spirurids. Strongylids and Strongyloides sp. have thin-shelled eggs and larvae, which develop in the external environment; thus they may not be able to survive for prolonged periods in the extreme environment of Ugalla. The Ugalla chimpanzees also live at a lower population density and exhibit a larger home range than forest chimpanzees, factors that may lead to lower exposure to infective nematode larvae. Spirurid eggs, however, have thick shells and a life cycle dependent on intermediary hosts, making their survival and transmission in such extreme conditions more feasible. These differences between parasite fauna of closed and open forest chimpanzees contribute to our understanding of the ecology of infectious disease, and have the potential to contribute to conservation policies and practices.

Keywords

Hominoid Pan troglodytes schweinfurthii Gastrointestinal parasites Savanna Spirurids Transmission Ugalla Tanzania 

References

  1. Anderson, R. C. (2000). Nematode parasites of vertebrates: Their development and transmission. Wallingford: CABI.CrossRefGoogle Scholar
  2. Appleton, C. C., & Brain, C. (1995). Gastrointestinal parasites of Papio cynocephalus ursinus living in the Central Namib Desert, Namibia. African Journal of Ecology, 33, 257–265.CrossRefGoogle Scholar
  3. Ash, L. R., & Orihel, T. C. (2007). Atlas of human parasitology. Singapore: American Society for Clinical Pathology Press.Google Scholar
  4. Ashford, R. W., Reid, G. D. F., & Wrangham, R. W. (2000). Intestinal parasites of the chimpanzee Pan troglodytes in Kibale Forest, Uganda. Annals of Tropical Medicine and Parasitology, 94, 173–179.PubMedCrossRefGoogle Scholar
  5. Bakuza, J. S., & Nkwengulila, G. (2009). Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania. International Journal of Primatology, 30, 43–53.CrossRefGoogle Scholar
  6. Baldwin, P. J., McGrew, W. C., & Tutin, C. E. G. (1982). Wide-ranging chimpanzees at Mt. Assirik, Senegal. International Journal of Primatology, 3, 367–385.CrossRefGoogle Scholar
  7. Benavides, J. A., Huchard, E., Pettorelli, N., King, A. J., Brown, M. E., Archer, C. E., et al. (2012). From parasite encounter to infection: Multiple-scale drivers of parasite richness in a wild social primate population. American Journal of Physical Anthropology, 147, 52–63.Google Scholar
  8. Bezjian, M., Gillespie, T. R., Chapman, C. A., & Greiner, E. C. (2008). Coprologic evidence of gastrointestinal helminths of forest baboons, Papio anubis, in Kibale National Park, Uganda. Journal of Wildlife Diseases, 44, 878–887.PubMedCrossRefGoogle Scholar
  9. Blagg, W., Schloegel, E. L., Mansour, N. S., & Khalaf, G. I. (1955). A new concentration technique for the demonstration of protozoa and helminth eggs in feces. The American Journal of Tropical Medicine and Hygiene, 4, 23–28.PubMedGoogle Scholar
  10. Boesch, C., Hohmann, G., & Marchant, L. (2002). Behavioral diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  11. Bogart, S. L., & Pruetz, J. D. (2011). Insectivory of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. American Journal of Physical Anthropology, 145, 11–20.PubMedCrossRefGoogle Scholar
  12. Bordes, F., Morand, S., Kelt, D. A., & Van Vurend, H. (2009). Home range and parasite diversity in mammals. The American Naturalist, 173, 467–474.PubMedCrossRefGoogle Scholar
  13. Boyce, M. S. (1990). Population viability analysis. Annual Review of Ecology and Systematics, 23, 481–406.CrossRefGoogle Scholar
  14. Brooks, D. R., & Ferrao, A. L. (2005). The historical biogeography of coevolution: Emerging infectious diseases are evolutionary accidents waiting to happen. Journal of Biogeography, 32, 1291–1299.CrossRefGoogle Scholar
  15. Caldecott, J., & Miles, L. (2005). World atlas of great apes and their conservation. Prepared at the UNEP World conservation monitoring centre. Berkeley: University of California Press.Google Scholar
  16. Cerling, T. E., Mbua, E., Kirera, F. M., Manthi, F. K., Grine, F. E., Leakey, M. G., et al. (2011). Diet of Paranthropus boisei in the early Pleistocene of east Africa. Proceedings of the National Academy of Science of the USA, 23, 9337–9341.Google Scholar
  17. Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T., & Austad, K. M. (2006). Life on the edge: Gastrointestinal parasites from the forest edge and interior primate groups. American Journal of Primatology, 68, 397–409.PubMedCrossRefGoogle Scholar
  18. Collins, D. A., & McGrew, W. C. (1988). Habitats of three groups of chimpanzees (Pan troglodytes) in western Tanzania compared. Journal of Human Evolution, 17, 553–574.CrossRefGoogle Scholar
  19. Diamond, L. S., & Clark, C. G. (1993). A redescription of Entamoeba histolytica Schaudinn, 1903 (emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. Journal of Eukaryotic Microbiology, 40, 340–344.PubMedCrossRefGoogle Scholar
  20. File, S. K., McGrew, W. C., & Tutin, C. E. G. (1976). The intestinal parasites of a community of feral chimpanzees (Pan troglodytes schweinfurthii). Journal of Parasitology, 62, 259–261.PubMedCrossRefGoogle Scholar
  21. Freeland, W. J. (1976). Panthogens and the evolution of primate sociality. Biotropica, 8, 12–24.CrossRefGoogle Scholar
  22. Ghandour, A. M., Zahid, N. Z., Banaja, A. A., Kamal, K. B., & Boug, A. L. (1995). Zoonotic intestinal parasites of hamadryas baboons Papio hamadryas in the western and northern regions of Saudi Arabia. Journal of Tropical Medicine and Hygiene, 98, 431–439.PubMedGoogle Scholar
  23. Gillespie, T. R., Nunn, C. L., & Leendertz, F. H. (2008). Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. American Journal of Physical Anthropology, 137, 53–69.CrossRefGoogle Scholar
  24. Glenn, D. R., & Brooks, D. R. (1986). Parasitological evidence pertaining to the phylogeny of the hominid primates. Biological Journal of the Linnean Society, 27, 331–354.CrossRefGoogle Scholar
  25. Hernandez-Aguilar, R. A. (2006). Ecology and nesting patterns of chimpanzees (Pan troglodytes) in Issa, Ugalla, Western Tanzania. Ph.D thesis, University of Southern California.Google Scholar
  26. Hernandez-Aguilar, R. A. (2009). Chimpanzee nest distribution and site reuse in a dry habitat: Implications for early hominin ranging. Journal of Human Evolution, 57, 350–364.PubMedCrossRefGoogle Scholar
  27. Hochachka, W. M., & Dhondt, A. (2000). Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Sciences of the USA, 97, 5303–5306.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hodder, S. A. M., & Chapman, C. A. (2012). Do nematode infections of red colobus (Procolobus rufomitratus) and black-and-white colobus (Colobus guereza) on humanized forest edges differ from those on nonhumanized forest edges? International Journal of Primatology, 33, 845–859.CrossRefGoogle Scholar
  29. Howells, M. E., Pruetz, J., & Gillespie, T. R. (2010). Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: The case of sympatric western (Papio hamadryas papio) at Fongoli, Senegal. American Journal of Primatology, 71, 1–7.Google Scholar
  30. Hudson, H. R. (1992). The relationship between stress and disease in orphan gorillas and its significance for gorilla tourism. Gorilla Conservation News, 6, 8–10.Google Scholar
  31. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H., & Dobson, A. P. (2002). The ecology of wildlife diseases. Oxford: Oxford University Press.Google Scholar
  32. Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M., & Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates, 38, 111–125.CrossRefGoogle Scholar
  33. Huffman, M. A., Pebsworth, P., Bakuneeta, C., Gotoh, S. G., & Bardi, M. (2009). Chimpanzee-parasite ecology at Budongo Forest (Uganda) and the Mahale Mountains (Tanzania): Influence of climatic differences on self-medicative behavior. In M. A. Huffman & C. Chapman (Eds.), Primate parasite ecology: The dynamics of host–parasite relationships (pp. 331–350). Cambridge: Cambridge University Press.Google Scholar
  34. Huffman, M. A., Petrželková, K. J., Moscovice, L. R., Issa, M. M., Bobáková, L., Mazoch, V., et al. (2008). Introduction of chimpanzees onto Rubondo Island National Park, Tanzania. In P. S. Soorae (Ed.), Global re-introduction Perspectives (pp. 213–216). Abu Dhabi: IUCN/SSC Re-introduction Specialist Group.Google Scholar
  35. Jessee, M. T., Schilling, P. W., & Stunkard, J. A. (1970). Identification of intestinal helminth eggs in old world primates. Laboratory Animal Care, 20, 83–87.PubMedGoogle Scholar
  36. Kano, T. (1972). Distribution and adaptation of the chimpanzees on the eastern shore of Lake Tanganyka. Kyoto University African Studies, 7, 37–129.Google Scholar
  37. Kaur, T., Singh, J., & Lindsay, D. S. (2010). Prevalence of Troglodytella abrassarti Brumpt and Joyeux, 1912 in Wild Chimpanzees (Pan troglodytes schweinfurthii) at Mahale Mountains National Park in Western Tanzania. Journal of Parasitology. 96, 209–210.Google Scholar
  38. Kawabata, M., & Nishida, T. (1991). A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains, Tanzania. Primates, 32, 275–278.CrossRefGoogle Scholar
  39. Kortland, A. (1983). Marginal habitats of chimpanzees. Journal of Human Evolution, 12, 231–278.CrossRefGoogle Scholar
  40. Krief, S., Huffman, M. A., Sevenet, T., Guillot, J., Bories, B., Hladik, C. M., et al. (2005). Non-invasive monitoring of the health of Pan troglodytes schweinfurthii in the Kibale National Park, Uganda. International Journal of Primatology, 26, 467–490.Google Scholar
  41. Landsoud-Soukate, J., Tutin, C. E., & Fernandez, M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lope Reserve, Gabon. Annals of Tropical Medicine and Parasitology, 89, 73–79.PubMedGoogle Scholar
  42. Lindenfors, P., Nunn, C. L., Jones, K. E., Cunningham, A. A., Sechrest, W., & Gittleman, J. L. (2007). Parasite species richness in carnivores: Effects of host body mass, latitude, geographical range and population density. Global Ecology and Biogeography, 1, 1–4.Google Scholar
  43. Matlack, G. R. (1993). Microenvironment variation within and among forest edge sites in the eastern United States. Biological Conservation, 66, 185–194.CrossRefGoogle Scholar
  44. McGrew, W. C. (1979). Evolutionary implications of sex differences in chimpanzee predation and tool use. In D. A. Hamburg & E. R. McCown (Eds.), The great apes (pp. 441–630). Menlo Park, CA: Benjamin/Cummings.Google Scholar
  45. McGrew, W. C., Tutin, C. E. G., Collins, D. A., & File, S. K. (1989). Intestinal parasites of sympatric Pan troglodytes and Papio spp., at two sites – Gombe (Tanzania) and Mt. Assirik (Senegal). American Journal of Primatology, 17, 147–155.CrossRefGoogle Scholar
  46. Modrý, D., Petrželková, K. J., Pomajbíková, K., Tokiwa, T., Křížek, J., Imai, S., et al. (2009). The occurrence and ape-to-ape transmission of the entodiniomorphid ciliates Troglodytella abrassarti in captive gorillas. Journal of Eucaryotic Microbiology, 56, 83–87.Google Scholar
  47. Mohr, C. O., & Stumpf, W. A. (1964). Relation of tick and chigger infestations to home areas of California meadow mice. Journal of Medical Entomology, 1, 73–77.PubMedGoogle Scholar
  48. Moore, J. (1992). “Savanna” chimpanzees. In T. Nishida, W. C. McGrew, P. Marler, M. P. Pickford, & F. B. M. Waal (Eds.), Topics in primatology: Human origins (pp. 99–118). Tokyo: University of Tokyo Press.Google Scholar
  49. Moore, J. (1994). Plants of the Tongwe East Forest Reserve (Ugalla), Tanzania. Tropics, 3, 333–340.CrossRefGoogle Scholar
  50. Moore, J. (1996). Savanna chimpanzees, referential models and the last common ancestor. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 275–292). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  51. Moscovice, L. R., Issa, M. H., Petrželková, K. J., Keuler, N. S., Snowdon, C. T., & Huffman, M. A. (2007). Fruit availability, chimpanzee diet, and grouping patterns on Rubondo Island, Tanzania. American Journal of Primatology, 69, 487–502.PubMedCrossRefGoogle Scholar
  52. Moyer, D., Plumptre, A. J., Pintea, L., Hernandez-Aguilar, A., Moore, J., Stewart, F., et al. (2006). Surveys of chimpanzees and other biodiversity in Western Tanzania. Report to United States Fish and Wildlife Service.Google Scholar
  53. Muehlenbein, M. P. (2005). Parasitological analyses of the 621 male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. American Journal of Primatology, 65, 167–179.PubMedCrossRefGoogle Scholar
  54. Murcia, C. (1995). Edge effects in fragmented forests: Implications for conservation. Trends in Ecology and Evolution, 10, 58–62.PubMedCrossRefGoogle Scholar
  55. Murray, S., Stem, C., Boudreau, B., & Goodall, J. (2000). Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park. Journal of Zoo and Wildlife Medicine, 31, 176–178.PubMedGoogle Scholar
  56. Myers, B. J., Kuntz, R. E., & Kamara, R. E. (1973). Parasites and commensals of chimpanzees captured in Sierra Leone, West Africa. Proceedings of the Helminthological Society of Washington, 40, 298–299.Google Scholar
  57. Nishida, T. (1989). A note on the chimpanzee ecology of the Ugalla area, Tanzania. Primates, 30, 129–138.CrossRefGoogle Scholar
  58. Nunn, C. L., & Altizar, S. (2006). Infectious diseases in primates: Behavior, ecology and evolution. New York: Oxford University Press.CrossRefGoogle Scholar
  59. Nunn, C. L., & Dokey, A. T. W. (2006). Ranging patterns and parasitism in primates. Biology Letters, 2, 351–354.PubMedCentralPubMedCrossRefGoogle Scholar
  60. Nunn, C. L., Thrall, P. H., Leendertz, F. H., & Boesch, C. (2011). The spread of fecally transmitted parasites in socially-structured population. PLoS One, 6, 21677.CrossRefGoogle Scholar
  61. Ogawa, H., Genich, I., Moore, J., Pintea, L., & Hernandez-Aguilar, R. A. (2007). Sleeping parties and nest distribution of chimpanzees in the savanna woodland, Ugalla, Tanzania. International Journal of Primatology, 28, 1397–1412.CrossRefGoogle Scholar
  62. Petrášová, J., Petrželková, K. J., Huffmen, M. A., Mapua, M. I., Bobáková, L., Mazoch, V., et al. (2010). Gastrointestinal parasites of indigenous and introduced primate species of Rubondo Island National Park, Tanzania. International Journal of Primatology, 31, 920–936.Google Scholar
  63. Petrželková, K. J., Hasegawa, H., Appleton, C. C., Huffman, M. A., Archer, C. E., Moscovice, L. R., et al. (2010). Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. American Journal of Primatology, 71, 1–10.Google Scholar
  64. Petrželková, K. J., Hasegawa, H., Moscovice, L. R., Kaur, T., Mapua, M. I., & Huffman, M. A. (2006). Parasitic nematodes in the chimpanzee population on Rubondo Island, Tanzania. International Journal of Primatology, 27, 767–777.CrossRefGoogle Scholar
  65. Piel, A. K., Stewart, F. A., Pintea, L., Li, Y., Ramirez, M. A., Loy, D. A., et al. (2013). The Malagarasi River does not form an absolute barrier to chimpanzee movement in western Tanzania. PLoS One, 8(3), e58965.Google Scholar
  66. Pomajbíková, K., Petrželková, K. J., Petrášová, J., Profousová, I., Kalousová, B., Jirků, M., et al. (2012). Distribution of the entodiniomorphid ciliate Troglocorys cava Tokiwa, Modrý, Ito, Pomajbíková, Petrželková, & Imai, (Entodiniomorphida: Blepharocorythidae) in wild and captive chimpanzees. Journal of Eukaryotic Microbiology, 59, 97–99.Google Scholar
  67. Pomajbíková, K., Petrželková, K. J., Profousová, I., Petrášová, J., Kišidayová, S., Varádyová, Z., et al. (2010). A survey of entodiniomorphid ciliates in chimpanzees and bonobos. American Journal of Physical Anthropology, 142, 42–48.Google Scholar
  68. Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43, 223–225.CrossRefGoogle Scholar
  69. Rudicell, R. S., Piel, A. K., Stewart, F., Moore, D. L., Learn, G. H., Li, Y. Y., et al. (2011). High prevalence of simian immunodeficiency virus infection in a community of savanna chimpanzees. Journal of Virology, 85, 9918–9928.Google Scholar
  70. Sheather, A. L. (1923). The detection of intestinal protozoa and mange parasites by a flotation technique. Journal of Comparative Pathology, 36, 266–275.CrossRefGoogle Scholar
  71. Skinner, M. F., & Pruetz, J. D. (2012). Reconstruction of periodicity of repetitive linear enamel hypoplasia from perikymata counts on imbricational enamel among dry-adapted chimpanzees (Pan troglodytes verus) from Fongoli, Senegal. American Journal of Physical Anthropology, 149, 468–482.PubMedCrossRefGoogle Scholar
  72. Smith, G. (1990). The population biology of the free-living phase of Haemonchus contortus. Parasitology, 101, 309–316.PubMedCrossRefGoogle Scholar
  73. Stewart, F. A. (2011). The evolution of shelter: Ecology and ethology of chimpanzee nest building. Ph.D thesis, University of Cambridge.Google Scholar
  74. Stewart, F. A., & Piel, A. K. (2013). Termite fishing by wild chimpanzees: New data from Ugalla, western Tanzania. Primates. Online in advance of print. doi: 10.1007/s10329-013-0362-6.
  75. Stoner, K. E. (1996). Prevalence and intensity of intestinal parasites in mantled howling monkeys (Alouatta palliata) in Northeastern Costa Rica: Implications for Conservation Biology. Conservation Biology, 10, 539–546.CrossRefGoogle Scholar
  76. Stuart, M. D., Pendergast, V., Rumfelt, S., Pierberg, S. M., Greenspan, L. L., Glander, K. E., et al. (1998). Parasites of wild howlers (Alouatta sp.). International Journal of Primatology, 19, 493–512.Google Scholar
  77. Tachibana, H., Cheng, X. J., Kobayashi, S., Fujita, Y., & Udono, T. (2000). Entamoeba dispar, but not E. histolytica, detected in a colony of chimpanzees in Japan. Parasitology Research, 86, 537–541.PubMedCrossRefGoogle Scholar
  78. Tokiwa, T., Modrý, D., Ito, A., Pomajbíková, K., Petrželková, K. J., & Imai, S. (2010). A new entodiniomorphid ciliate, Troglocorys cava n. g., n. sp., from the wild eastern chimpanzee (Pan troglodytes schweinfurthii) from Uganda. Journal of Eucaryotic Microbiology, 57, 115–120.CrossRefGoogle Scholar
  79. Uehara, S. (1986). Sex and group differences in feeding on animals by wild chimpanzees in the Mahale Mountains National Park, Tanzania. Primates, 27, 1–13.CrossRefGoogle Scholar
  80. Verweij, J. J., Polderman, A. M., & Clark, C. G. (2001). Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. Journal of Clinical Microbiology, 39, 1644–1646.PubMedCentralPubMedCrossRefGoogle Scholar
  81. Yamagiwa, J. (2004). Diet and foraging of the great apes: Ecological constraints on their social organizations and implications for their divergence. In A. E. Russon & D. R. Begun (Eds.), The evolution of thought: Evolutionary origins of great ape intelligence (pp. 210–233). Cambridge: Cambridge University Press.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Barbora Kalousová
    • 1
    • 2
  • Alexander K. Piel
    • 3
    • 4
  • Kateřina Pomajbíková
    • 1
    • 5
  • David Modrý
    • 1
    • 5
  • Fiona A. Stewart
    • 4
  • Klára J. Petrželková
    • 1
    • 5
    • 6
    • 7
  1. 1.Department of Pathology and Parasitology, Faculty of Veterinary Medicine, and CEITEC-Central European Institute of TechnologyUniversity of Veterinary and Pharmaceutical SciencesBrnoCzech Republic
  2. 2.Department of Botany and ZoologyMasaryk UniversityBrnoCzech Republic
  3. 3.Department of AnthropologyUniversity of CaliforniaLa JollaUSA
  4. 4.Department of Archaeology and Anthropology, Division of Biological AnthropologyUniversity of CambridgeCambridgeU.K.
  5. 5.Institute of ParasitologyAcademy of Sciences of the Czech RepublicČeské BudějoviceCzech Republic
  6. 6.Institute of Vertebrate BiologyAcademy of Sciences of the Czech Republic, v.v.i.BrnoCzech Republic
  7. 7.Liberec ZooLiberecCzech Republic

Personalised recommendations