International Journal of Primatology

, Volume 28, Issue 3, pp 593–606 | Cite as

Influence of Chimpanzee Predation on Associations Between Red Colobus and Red-tailed Monkeys at Ngogo, Kibale National Park, Uganda

Special Issue: Behavior, Ecology, and Conservation of Colobine Monkeys

Abstract

Colobines often associate with cercopithecines at various African sites. Such polyspecific associations presumably have an antipredation function. At Ngogo, Kibale National Park, Uganda, red colobus (Procolobus rufomitratus) spend considerable time in association with red-tailed monkeys (Cercopithecus ascanius), and they are also heavily hunted by chimpanzees (Pan troglodytes). I conducted behavioral observations and playback experiments to test the hypothesis that red colobus and red-tailed monkeys obtain mutual protection and predator-related benefits by associating. Despite high chimpanzee hunting pressure on red colobus and much lower hunting pressure on red-tailed monkeys, red-tailed monkeys initiate, maintain, and terminate the associations. The results suggest that rather than providing red colobus with protection against chimpanzees, the associations occur mostly because they protect red-tailed monkeys against predation by eagles.

Keywords

hunting Kibale National Park polyspecific associations red colobus monkeys red-tailed monkeys 

Notes

Acknowledgments

I thank David Watts and John Mitani for their help with this study, their constructive comments and much more. Tom Struhsaker, Colin Chapman, and 1 anonymous reviewer provided valuable comments on an earlier version of the manuscript. In addition, I particularly thank Stephanie F. Anestis, Jeremiah S. Lwanga, and Marianne Pouplier. Furthermore, my thanks go to Tammy Windfelder, and the people at Ngogo, all of whom had some kind of impact at some point in time on this study: Businge Charles, Kabagambe Dominique, Magambo Norris, Magoba Adolph, Mbabazi Godfrey, Ndanhizi Lawrence, Tibisimwa James, and Tumusiime Alfred. The Leakey Foundation, the National Science Foundation (dissertation improvement grant BCS-0109999), and the Enders Foundation funded the study. The Office of the President in Uganda, the National Council for Science and Technology in Uganda, Ugandan Wildlife Authority, Makerere University Biological Field Station, and Yale’s Animal Care and Use Committee granted permission.

References

  1. Boesch, C. (1994). Chimpanzees-red colobus monkeys: A predator-prey system. Animal Behavior, 47, 1135–1148.CrossRefGoogle Scholar
  2. Boesch, C., & Boesch, H. (1989). Hunting behavior of wild chimpanzees in the Taï National Park. American Journal of Physical Anthropology, 78, 547–573.PubMedCrossRefGoogle Scholar
  3. Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taï Forest - Behavioural ecology and evolution. Oxford: Oxford University Press.Google Scholar
  4. Bshary, R., & Noë, R. (1997a). Anti-predation behaviour of red colobus monkeys in the presence of chimpanzees. Behavioral Ecology and Sociobiology, 41, 321–333.CrossRefGoogle Scholar
  5. Bshary, R., & Noë, R. (1997b). Red colobus and diana monkeys provide mutual protection against predators. Animal Behavior, 54, 1461–1474.CrossRefGoogle Scholar
  6. Chapman, C. A., & Chapman, L. J. (1996). Mixed-species primate groups in the Kibale forest: Ecological constraints on association. International Journal of Primatology, 17, 31–50.Google Scholar
  7. Chapman, C. A., & Chapman, L. J. (2000). Interdemic variation in mixed-species association patterns: common diurnal primates of Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 47, 129–139.CrossRefGoogle Scholar
  8. Chapman, C. A., & Chapman, L. J. (2002). Foraging challenges for red colobus monkeys: Influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology, 133, 861–875.PubMedGoogle Scholar
  9. Cheney, D. L., & Wrangham, R. W. (1987). Predation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker (Eds.), Primate Societies (pp. 429-450). Chicago and London: University of Chicago Press.Google Scholar
  10. Clutton-Brock, T., & Harvey, P. (1977). Primate ecology and social organization. Journal of Zoology, 183, 1–39.CrossRefGoogle Scholar
  11. Cords, M. (1987). Mixed-species association of Cercopithecus monkeys in the Kakamega Forest, Kenya. Berkeley, CA: University of California Publications in Zoology.Google Scholar
  12. Cords, M. (1990a). Mixed-species association of East African guenons: General patterns or specific examples? American Journal of Primatology, 21, 101–114.CrossRefGoogle Scholar
  13. Cords, M. (1990b). Vigilance and mixed-species association of some east-African forest monkeys. Behavioral Ecology and Sociobiology, 26, 297–300.CrossRefGoogle Scholar
  14. Eckardt, W., & Zuberbühler, K. (2004). Cooperation and competition in two forest monkeys. Behavioral Ecology, 15, 400–411.CrossRefGoogle Scholar
  15. Gautier-Hion, A., Quris, R., & Gautier, J.-P. (1983). Monospecific vs polyspecific life: a comperative study of foraging and antipredatory tactics in a community of Cercopithecus monkeys. Behavioral Ecology and Sociobiology, 12, 325–335.CrossRefGoogle Scholar
  16. Ghiglieri, M. P. (1984). The Chimpanzees of the Kibale Forest. New York: Columbia University Press.Google Scholar
  17. Holenweg, A.-K., Noë, R., & Schabel, M. (1996). Waser’s gas model applied to associations between red colobus and Diana Monkeys in the Taï National Park, Ivory Coast. Folia Primatologica, 67, 125–136.Google Scholar
  18. Hoseka, K., Nishida, T., Hamai, M., Matsumoto-Oda, A., & Uehara S. (2001). Predation of mammals by chimpanzees of the Mahale Mountains, Tanzania. In B. Galdikas, N. Briggs, L. Sheeran, G. Shapiro, & J. Goodall, (Eds), All apes great and small (pp. 107–130). New York: Kluwer Academic.Google Scholar
  19. Janson, C. H., & Goldsmith, M. L. (1995). Predicting group size in primates: Foraging costs and predation risks. Behavioral Ecology, 6, 326–336.CrossRefGoogle Scholar
  20. Leland, L., & Struhsaker, T. T. (1993). Teamwork tactics. Natural History, 102, 42–48.Google Scholar
  21. Lwanga, J. S. (2003). Forest succession in Kibale National Park, Uganda: Implications for forest restoration and management. African Journal of Ecology, 41, 9–22.CrossRefGoogle Scholar
  22. Lwanga, J. S., Butynski, T. M., & Struhsaker, T. T. (2000). Tree population dynamics in Kibale National Park, Uganda 1975–1998. African Journal of Ecology, 38, 238–247.CrossRefGoogle Scholar
  23. McGraw, W. S. (1994). Census, habitat preference, and polyspecific associations of six monkeys in the Lomako Forest, Zaire. American Journal of Primatology, 34, 295–307.CrossRefGoogle Scholar
  24. McGraw, W. S. (1998). Comparative locomotion and habitat use of six monkeys in the Taï Forest, Ivory Coast. American Journal of Physical Anthropology, 105, 493–510.PubMedCrossRefGoogle Scholar
  25. McGraw, W. S., & Bshary, R. (2002). Association of terrestrial mangabeys (Cercocebus atys) with arboreal monkeys: Experimental evidence for the effects of reduced ground predator pressure on habitat use. International Journal of Primatology, 23, 311–325.CrossRefGoogle Scholar
  26. Mitani, J. C., & Watts, D. P. (1999). Demographic influences on the hunting behavior of chimpanzees. American Journal of Physical Anthropology, 109, 439–454.PubMedCrossRefGoogle Scholar
  27. Mitani, J. C., Sanders, W. J., Lwanga, J. S., & Windfelder, T. L. (2001). Predatory behavior of crowned hawk-eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 49, 187–195.CrossRefGoogle Scholar
  28. Mitani, J. C., Struhsaker, T. T., & Lwanga, J. S. (2000). Primate community dynamics in old growth forest over 23.5 years at Ngogo, Kibale National Park, Uganda: Implications for conservation and census methods. International Journal of Primatology, 21, 269–286.CrossRefGoogle Scholar
  29. Noë, R., & Bshary, R. (1997). The formation of red colobus-Diana monkey associations under predation pressure from chimpanzees. Proceedings of the Royal Society of London — Series B: Biological Sciences, 264, 253–259.CrossRefGoogle Scholar
  30. Oates, J. F., & Whitesides, G. H. (1990). Association between olive colobus (Procolobus versus), Diana guenons (Cercopithecus diana), and other forest monkeys in Sierra Leone. American Journal of Primatology, 21, 129–146.CrossRefGoogle Scholar
  31. Oates, J. F., Whitesides, G. H. Davies, A. G., Waterman, P. G., Green, S. M., Dasilva, G. L. et al. (1990). Determinants of variation in tropical forest primate biomass: new evidence from West Africa. Ecology, 71, 328–343.CrossRefGoogle Scholar
  32. Porter, L. M. (2001). Benefits of polyspecific associations for the goeldi’s monkey (Callimico goeldii). American Journal of Primatology, 54, 143–158.PubMedCrossRefGoogle Scholar
  33. Sanders, W. J., Trapani, J., & Mitani, J. C. (2003). Taphonomic aspects of crowned hawk-eagle predation on monkeys. Journal of Human Evolution, 44, 87–105.PubMedCrossRefGoogle Scholar
  34. Shultz, S. (2001). Notes on interactions between monkeys and African crowned eagles in Taï National Park, Ivory Coast. Folia Primatologica, 72, 248–250.CrossRefGoogle Scholar
  35. Shultz, S., & Noë, R. (2002). The consequences of crowned eagle central-place foraging on predation risk in monkeys. Proceedings of the Royal Society of London — Series B: Biological Sciences, 269, 1797–1802.PubMedCrossRefGoogle Scholar
  36. Shultz, S., Noë, R., McGraw, W. S., & Dunbar, R. I. M. (2004). A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition. Proceedings of the Royal Society of London-Series B: Biological Sciences, 271, 725–732.PubMedCrossRefGoogle Scholar
  37. Skorupa, J. P. (1989). Crowned Eagle Stephanoaetus coronatus in rainforests: Observations on breeding chronology and diet at a nest in Uganda. IBIS, 131, 294–298.Google Scholar
  38. Stanford, C. B. (1995). The influence of chimpanzee predation on group size and anti-predator behavior in red colobus monkeys. Animal Behavior, 49, 577–587.Google Scholar
  39. Stanford, C. B. (1998). Chimpanzee and red colobus: The ecology of predator and prey. Cambridge, MA: Harvard University Press.Google Scholar
  40. Stanford, C. B., Wallis, J., Matama, H., & Goodall, J. (1994). Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, 1982–1991. American Journal of Primatology, 94, 213–228.Google Scholar
  41. Stensland, E., Angerbjorn, A., & Berggren, P. (2003). Mixed species groups in mammals. Mammal Review, 33, 205–223.CrossRefGoogle Scholar
  42. Struhsaker, T. T. (1978). Food habits of five monkey species in the Kibale Forest, Uganda. In D. J. Chivers & J. Herbert (Eds.), Recent advances in primatology (pp. 225–248). London: Academic Press.Google Scholar
  43. Struhsaker, T. T. (1981). Polyspecific association among tropical rain-forest primates. Zeitschrift für Tierpsychologie, 57, 268–304.Google Scholar
  44. Struhsaker, T. T. (1997). Ecology of an African Rain Forest-Logging in Kibale and the Conflict between Conservation and Exploitation. Gainsville, FL: University Press of Florida.Google Scholar
  45. Struhsaker, T. T. (2000). The effects of predation and habitat quality on the socioecology of African monkeys: lessons from the islands of Bioko and Zanzibar. In P. F. Whitehead & C. J. Jolly (Eds.), Old World Monkeys (pp. 393–430). Cambridge, UK: Cambridge University Press.Google Scholar
  46. Struhsaker, T. T., & Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys in the Kibale Forest, Uganda. Behavioral Ecology and Sociobiology, 26, 435–444.CrossRefGoogle Scholar
  47. Struhsaker, T. T., & Leland, L. (1979). Socioecology of five sympatric monkey species in the Kibale Forest, Uganda. Advances in the Study of Behavior, 9, 159–228.CrossRefGoogle Scholar
  48. Teelen, S. (2005). The impact of hunting by chimpanzees (Pan troglodytes) on demography and behavior of red colobus monkeys (Procolubus rufomitratus) at Ngogo, Kibale National Park, Uganda. [PhD]. New Haven, CT: Yale University.Google Scholar
  49. Teelen, S. (2007). Primate abundance along five transect lines at Ngogo, Kibale National Park, Uganda. American Journal of Primatology. DOI  10.1002/ajp.20417.
  50. Terborgh, J. (1983). Five new world primates: A study in comperative ecology. Princeton University Press.Google Scholar
  51. Terborgh, J. (1990). Mixed flocks and polyspecific associations: costs and benefits of mixed groups to birds and monkeys. American Journal of Physical Anthropology, 21, 87–100.Google Scholar
  52. Terborgh, J., & Janson, C. H. (1986). The socioecology of primate groups. Annual Reviews of Ecological Systems, 17, 111–135.CrossRefGoogle Scholar
  53. Treves, A. (1997). Self-Protection in Primates. [PhD]. Cambridge, MA: Harvard University.Google Scholar
  54. van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.). Comparative Socioecology–– The Behavioural Ecology of Humans and Other Mammals (pp. 195–218). Oxford: Blackwell.Google Scholar
  55. van Schaik, C. P., & van Hooff, J. A. R. A. M. (1983). On the ultimate causes of primate social systems. Behaviour, 85, 91–117.Google Scholar
  56. Wachter, B., Schabel, M., & Noë, R. (1997). Diet overlap and polyspecific associations of red colobus and Diana monkeys in the Taï National Park, Ivory Coast. Ethology, 103, 514–526.CrossRefGoogle Scholar
  57. Waser, P. (1982). Polyspecific associations: do they occur by chance? Animal Behavior, 30, 1–8.CrossRefGoogle Scholar
  58. Waser, P. (1984). “Chance” and mixed-species associations. Behavioral Ecology and Sociobiology, 15, 197–202.CrossRefGoogle Scholar
  59. Waser, P. M. (1987). Interactions among primate species. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker (Eds.), Primate societies (pp. 210–226). Chicago: University of Chicago Press.Google Scholar
  60. Watts, D. P., & Mitani, J. C. (2002) Hunting behavior of chimpanzee at Ngogo, Kibale National Park, Uganda. International Journal of Primatology, 23, 1–28.CrossRefGoogle Scholar
  61. Windfelder, T. L., & Lwanga, J. S. (2002). Mixed species associations of redtail monkeys (Cercopithecus ascanius) and mangabeys (Lophocebus albigena) at the Ngogo study site, Kibale National Park, Uganda. American Journal of Primatology, 56, 65–66.CrossRefGoogle Scholar
  62. Wolters, S., & Zuberbühler, K. (2003). Mixed-species associations of Diana and Campbell's monkeys: The costs and benefits of a forest phenomenon. Behaviour, 140, 371–385.CrossRefGoogle Scholar
  63. Wrangham, R. W., & Riss, E. V. Z. B. (1990). Rates of predation on mammals by Gombe chimpanzees,1972–1975. Primates, 31, 157–170.CrossRefGoogle Scholar
  64. Zuberbühler, K., Noë, R., & Seyfarth, R. M. (1997). Diana monkey long distance calls: Messages for conspecifics and predators. Animal Behavior, 53, 589–604.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Yale UniversityNew HavenUSA

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