Avoiding Predators: Expectations and Evidence in Primate Antipredator Behavior

International Journal of Primatology volume 23, pages741–757(2002)Cite this article

Abstract

Predation and antipredator behavior are important but poorly studied influences on the evolution of primate societies. I review recent evidence of predation and antipredator strategies among primates. I describe patterns of antipredator behavior and attempt to explain the variation among primate taxa and among antipredator strategies. I use predation by chimpanzees on red colobus and antipredator strategies by the colobus as a case study of how a primate prey species may respond to the threat of predation.

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REFERENCES

  1. Abrams, P. A. (1994). Should prey overestimate the risk of predation? Am. Nat. 144: 317–328.

    Google Scholar 

  2. Altmann, J. (2000). Models of outcome and process: Predicting the number of males in primate groups. In Kappeler, P. M. (ed.), Primate Males Cambridge University Press, Cambridge, pp. 236–247.

    Google Scholar 

  3. Anderson, C. M. (1986). Predation and primate evolution. Primates 27: 15–39.

    Google Scholar 

  4. Baldellou, M. B., and Henzi, P. (1992). Vigilance, predator detection and the presence of supernumerary males in vervet monkey troops. Anim. Behav. 43: 451–461.

    Google Scholar 

  5. Barnard, C. J. (1981). Factors affecting flock size mean and variance in a winter population of house sparrows. Behaviour 74: 114–127.

    Google Scholar 

  6. Bartecki, U., and Heymann, E. W. (1987). Field observation of snake-mobbing in a group of saddle-back tamarins, Saguinus fuscicollis nigrifrons. Folia Primatol. 48: 199–202.

    Google Scholar 

  7. Bertram, B. C. R. (1980). Vigilance and group size in ostriches. Anim. Behav. 28: 278–286.

    Google Scholar 

  8. Boinski, S. (1989).Why don't Saimiri oerstedii and Cebus capucinus form mixed-species groups? Int. J. Primatol. 30: 85–100.

    Google Scholar 

  9. Boinski, S., and Chapman, C. A. (1995). Predation on primates:Where are we and what next? Evol. Anthropol. 4: 1–13.

    Google Scholar 

  10. Boinski, S., Treves, A., and Chapman, C. A. (2000). A critical evaluation of the influence of predators on primates: Effects of group travel. In Boinski, S., and Garber, P. A. (eds.), On the Move: How and Why Animals Travel in Groups University of Chicago Press, Chicago, pp. 43–72.

    Google Scholar 

  11. Bshary, R., and Noë , R. (1997). Antipredation behaviour of red colobus monkeys in the presence of chimpanzees. Behav. Ecol. Sociobiol. 41: 321–333.

    Google Scholar 

  12. Busse, C. D. (1977). Chimpanzee predation as a possible factor in the evolution of red colobus monkey social organization. Evolution 31: 907–911.

    Google Scholar 

  13. Chapman, C. A. (1986). Boa constrictor predation and group response in white-faced cebus.Biotropica 18: 171–172.

    Google Scholar 

  14. Charnov, E. L., and Krebs, J.R. (1975). The evolution of alarm calls: Altruism or manipulation? Am. Nat. 109: 107–112.

    Google Scholar 

  15. Cheney, D. L., and Seyfarth, R. M. (1981). Selective forces affecting the predator alarm call of vervet monkeys. Behaviour 76: 25–61.

    Google Scholar 

  16. Cheney, D. L., and Seyfarth, R. M. (1990). How Monkeys See theWorld, University of Chicago Press, Chicago.

    Google Scholar 

  17. Cheney, D. L., Seyfarth, R. M., Andelman, S. J., and Lee, P. C. (1988). Reproductive success in vervet monkeys. In Clutton-Brock, T. H. (ed.), Reproductive Success, University of Chicago Press, Chicago, pp. 384–402.

    Google Scholar 

  18. Cheney, D. L., and Wrangham, R.W. (1987). Predation. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 227–239.

    Google Scholar 

  19. Clutton-Brock, T. H., and Harvey, P.H. (1977). Primate ecology and social organization. J. Zool. 183: 1–39.

    Google Scholar 

  20. Condit, V. K., and Smith, E. O. (1994). Predation on a yellow baboon (Papio cynocephalus cynocephalus) by a lioness in the Tana River National Primate Reserve, Kenya. Am. J.Primatol. 33: 57–64.

    Google Scholar 

  21. Cords, M. (1990).Vigilance and mixed-species association of some East African forest monkeys.Behav. Ecol. Sociobiol. 26: 297–300.

    Google Scholar 

  22. Cowlishaw, G. (1997). Trade-offs between foraging and predation risk determine habitat use in a desert baboon population. Anim. Behav. 53: 667–686.

    Google Scholar 

  23. Csermely, D. (1996). Antipredator behavior in lemurs: Evidence of an extinct eagle on Madagascar or something else? Int. J. Primatol. 17: 349–254.

    Google Scholar 

  24. Curio, E. (1978). The adaptive significance of avian mobbing: I. Teleonomic hypotheses and predictions. Z. Tierpsychol. 48: 175–183.

    Google Scholar 

  25. de Ruiter, J.R. (1986). The influence of group size on predator scanning and foraging behaviour of wedgecapped capuchin monkeys (Cebus olivaceus). Behaviour 98: 240–258.

    Google Scholar 

  26. Elgar, M. A. (1989). Predator vigilance and group size in mammals and birds: A critical review of the empirical evidence. Biol. Rev. 64: 13–33.

    Google Scholar 

  27. Fay, J. M., Carroll, R., Kerbis Peterhans, J. C., and Harris, D. (1995). Leopard attack and consumption of gorillas in the Central African Republic. J. Hum. Evol. 29: 93–99.

    Google Scholar 

  28. Fitzgibbon, C. D. (1990). Mixed-species grouping in Thompson's and Grant's gazelles: The antipredator benefits. Anim. Behav. 39: 1116–1126.

    Google Scholar 

  29. Gautier-Hion, A., Quris, R., and Gautier, J. P. (1983). Monospecific vs. polyspecific life: A comparative study of foraging and antipredatory tactics in a community of Cercopithecus monkeys. Behav. Ecol. Sociobiol. 12: 325–335.

    Google Scholar 

  30. Goodman, S. M. (1994). The enigma of anti-predator behavior in lemurs: Evidence of a large extinct eagle on Madagascar. Int. J. Primatol. 15: 129–134.

    Google Scholar 

  31. Goodman, S. M., O'Connor, S., and Langrand, O. (1993). A review of predation on lemurs: Implications for the evolution of social behavior in small, nocturnal primates. In Kappeler, P. M., and Ganzhorn, J.U. (eds.), Lemur Social Systems and their Ecological Basis, Plenum Press, New York, pp. 51–66.

    Google Scholar 

  32. Haftorn, S. (2000). Contexts and possible functions of alarm calling in the willow tit, Parus montanus; the principle of "better safe than sorry." Behaviour 137: 437–449.

    Google Scholar 

  33. Hamilton, W. D. (1971). Geometry for the selfish herd. J. Theor. Biol. 31: 295–311.

    Google Scholar 

  34. Heymann, E., and Buchanan-Smith, H. (2000).The behavioural ecology of mixed-species troops of callitrichine primates. Biol. Rev. 75: 169–190.

    Google Scholar 

  35. Hill, R., and Dunbar, R. I.M. (1998). An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour 135: 411–430.

    Google Scholar 

  36. Hill, R. A., and Lee, P. C. (1998). Predation risk as an influence on group size in cercopithecoid primates: Implications for social structure. J. Zool. 245: 447–456.

    Google Scholar 

  37. Hogstad, O. (1995). Alarm calling by willow tits, Parus montanus, as mate investment. Anim.Behav. 49: 221–225.

    Google Scholar 

  38. Isbell, L. A. (1994). Predation on primates: Ecological patterns and evolutionary consequences.Evol. Anthropol. 3: 61–71.

    Google Scholar 

  39. Janson, C. H. (1992). Evolutionary Ecology of primate social structure. In by Smith, E. A., and Winterhalder, B. (eds.), Evolutionary Ecology and Human Behavior, Aldine, New York, pp. 95–130.

    Google Scholar 

  40. Janson, C. H. (1998). Testing the predation hypothesis for vertebrate sociality: Prospects and pitfalls. Behaviour 135: 389–410.

    Google Scholar 

  41. Janson, C. H., and Goldsmith, M. L. (1995). Predicting group size in primates: Foraging costs and predation risks. Behav. Ecol. 6: 326–336.

    Google Scholar 

  42. Karpanty, S. M., and Goodman, S. M. (1999). Diet of the Madagascar harrier-hawk (Poloyboroides radiatus) in southeastern Madagascar. J. Raptor Res. 33: 313–316.

    Google Scholar 

  43. LaGory, K. E. (1987). The influence of habitat and group characteristics on the alarm calls and flight response of white-tailed deer. Anim. Behav. 35: 20–25.

    Google Scholar 

  44. Lima, S. L. (1995). Back to the basics of anti-predatory vigilance: The group-size effect. Anim.Behav. 49: 11–20.

    Google Scholar 

  45. Lima, S. L., and Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Can. J. Zool. 68: 619–640.

    Google Scholar 

  46. Macedonia, J. M. (1990).What is communicated in the antipredator calls of lemurs? Evidence from playback experiments with ringtailed and ruffed lemurs. Ethology 86: 177–190.

    Google Scholar 

  47. Mitani, J. C., and Brandt, K. L. (1994). Social factors influence the acoustic variability in the the long-distance calls of male chimpanzees. Ethology 96: 233–252.

    Google Scholar 

  48. Mitani, J. C., Gros-Louis, J., and Manson, J. H. (1996). Number of males in primate groups: Comparative tests of competing hypotheses. Am. J. Primatol. 38: 315–332.

    Google Scholar 

  49. Mitani, J. C., Sanders, W. J., Lwanga, J. S., and Windfelder, T. L. (2001). Predatory behavior of crowned hawk-eagles (Stephanoetus coronatus) in Kibale National Park, Uganda. Behav.Ecol. Sociobiol. 49: 187–195.

    Google Scholar 

  50. Mø ller, A. P. (1988). False alarm calls as a means of resource usurpation in the great tit Parus major. Ethology 79: 25–30.

    Google Scholar 

  51. Moynihan, M. (1962). The organization and probable evolution of some mixed species flocks of neotropical birds. Smiths. Misc. Coll. 143: 1–40.

    Google Scholar 

  52. Munn, C. A. (1985). Permanent canopy and understory flocks in Amazonia: Species composition and population density. In Buckley, P. A., Foster, M. S., Morton, E. S., Ridgely, R. S., and Buckley, F. G. (eds.), Neotropical Ornithology, America Ornithological Union, New York, Ornithological Monographs, Vol. 36, pp. 683–712.

    Google Scholar 

  53. Nöe, R., and Bshary, R. (1997). The formation of red colobus-diana monkey associations under predation pressure from chimpanzees. Proc. R. Soc. Lond. B 264: 253–259.

    Google Scholar 

  54. Owings, D. H., and Hennessy, D. F. (1984). The importance of variation in sciurid visual and vocal communication. In Murie, J. O., and Michener, G. R. (eds.), The Biology of Ground-Dwelling Squirrels, University of Nebraska Press, Lincoln, NE, pp. 169–200.

    Google Scholar 

  55. Passamani, M. (1995). Field observation of a group of Geoffroy's marmosets mobbing a margay cat. Folia Primatol. 64: 163–166.

    Google Scholar 

  56. Pereira, M. E., and Macedonia, J. M. (1991). Ringtailed lemur anti-predator calls denote predator class, not response urgency. Anim. Behav. 41: 543–544.

    Google Scholar 

  57. Peres, C. A. (1993). Anti-predation benefits in a mixed species groups of tamarins. Folia Primatol. 61: 61–76.

    Google Scholar 

  58. Pook, A.G., and Pook, G. (1982).Polyspecific association between Saguinus fuscicollis, Saguinus labiatus and Callimico goeldii and other primates in north-western Bolivia. Folia Primatol. 38: 196–216.

    Google Scholar 

  59. Pulliam, H. R. (1973). On the advantages of flocking. J. Theor. Biol. 38: 419–422.

    Google Scholar 

  60. Pulliam, H. R., and Caraco, T. (1984). Living in groups: Is there an optimal group size? In Krebs, J. R., and Davies, N. B. (eds.), Behavioural Ecology: An Evolutionary Approach, Blackwell Scientific, London, pp. 122–147.

    Google Scholar 

  61. Rasoloarison, R., Goodman, S., and Ganzhorn, J. (2000).Ataxonomic revision of mouse lemurs (Microcebus) occurring in the western portions of Madagascar. Int. J. Primatol. 21: 963–1019.

    Google Scholar 

  62. Rasoloarison, R., Rasolonandrasana, B., Ganzhorn, J., and Goodman, S. (1995). Predation on vertebrates in the Kirindy forest, western Madagascar. Ecotropica 1: 59–65.

    Google Scholar 

  63. Rettig, N. L. (1978). Breeding behavior of the harpy eagle (Harpia harpyia). Auk 95: 629–643.

    Google Scholar 

  64. Rose, L., and Fedigan, L. M. (1995). Vigilance in white-faced capuchins, Cebus capucinus, in Costa Rica. Anim. Behav. 49: 63–70.

    Google Scholar 

  65. van Schaik, C. P. (1983).Why are diurnal primates living in groups? Behaviour 87: 120–144.

    Google Scholar 

  66. van Schaik, C. P., and Hörstermann, M. (1994). Predation risk and the number of adult males in a primate group: A comparative test. Behav. Ecol. Sociobiol. 35: 261–272.

    Google Scholar 

  67. van Schaik, C. P., and van Noordwijk, M. A. (1985). Evolutionary effect of the absence of felids on the social organization of the macaques on the island of Simeulue (Macaca fascicularis, Miller 1903). Folia Primatol. 44: 138–147.

    Google Scholar 

  68. van Schaik, C. P., and van Noordwijk, M. A. (1989). The special role of male Cebus monkeys in predation avoidance and its effect on group composition. Behav. Ecol. Sociobiol. 24: 265–276.

    Google Scholar 

  69. Schaller, G. (1967). The Deer and the Tiger, University of Chicago Press, Chicago.

    Google Scholar 

  70. Scheel, D. (1993). Profitability, encounter rates, and prey choice of African lions. Behav. Ecol. 4: 90–97.

    Google Scholar 

  71. Schleidt, W. M. (1973). Tonic communication: Continual effects of discrete signs in animal communication. J. Theor. Biol. 42: 359–386.

    Google Scholar 

  72. Sherman, P.W. (1977). Nepotism and the evolution of alarm calls. Science 197: 1246–1253.

    Google Scholar 

  73. Sherman, P.W. (1985). Alarm calls of Belding's ground squirrels to aerial predators: Nepotism or self-preservation? Behav. Ecol. Sociobiol. 17: 313–324.

    Google Scholar 

  74. Skorupa, J. (1989). Crowned eagles (Stephanoetus coronatus) in rainforest: Observations on breeding chronology and diet at a nest in Uganda. Ibis 131: 294–298.

    Google Scholar 

  75. Stanford, C. B. (1989). Predation by jackals (Canis aureus) on capped langurs (Presbytis pileata) in Bangladesh. Am. J. Primatol. 18: 53–56.

    Google Scholar 

  76. Stanford, C. B. (1995). The influence of chimpanzee predation on group size and anti-predator behaviour in red colobus monkeys. Anim. Behav. 49: 577–587.

    Google Scholar 

  77. Stanford, C. B. (1998a). Chimpanzee and Red Colobus: The Ecology of Predator and Prey, Harvard University Press, Cambridge, MA.

    Google Scholar 

  78. Stanford, C.B. (1998b). Predation and male bonds in primate societies. Behaviour 135: 513–533.

    Google Scholar 

  79. Stanford, C. B., Wallis, J., Matama, H., and Goodall, J. (1994). Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, Tanzania, 1982- 1991. Am. J.Phys. Anthropol. 94: 213–228.

    Google Scholar 

  80. Steenbeek, R., Assink, P., van Buul, M., and van Hooff, J. A. R. A. M. (1999). Vigilance in wild Thomas' langurs (Presbytis thomasi): The importance of predation risk. Behav. Ecol.Sociobiol. 45: 137–150.

    Google Scholar 

  81. Struhsaker, T. T. (1975). The Red Colobus Monkey, University of Chicago Press, Chicago.

    Google Scholar 

  82. Struhsaker, T. T., and Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys in the Kibale Forest, Uganda. Behav. Ecol. Sociobiol. 26: 435–443.

    Google Scholar 

  83. Sullivan, K. A. (1984). The advantages of social foraging in downy woodpeckers. Anim. Behav. 32: 16–22.

    Google Scholar 

  84. Terborgh, J. (1983). Five New World Primates, Princeton University Press, Princeton, NJ.

    Google Scholar 

  85. Terborgh, J. (1990). Mixed flocks and polyspecific associations: Costs and benefits of mixed groups to birds and monkeys. Am. J. Primatol. 21: 87–100.

    Google Scholar 

  86. Terborgh, J., and Janson, C. H. (1986). The socioecology of primate groups. Annu. Rev. Ecol.Syst. 17: 111–135.

    Google Scholar 

  87. Treves, A. (1999). Has predation shaped the social systems of arboreal primates? Int. J. Primatol. 20: 35–67.

    Google Scholar 

  88. Tsukahara, T. (1993). Lions eat chimpanzees: The first evidence of predation by lions on wild chimpanzees. Am. J. Primatol. 29: 1–11.

    Google Scholar 

  89. Tutin, C. E.G., McGrew, W.C., and Baldwin, P. J. (1981). Social organization of savanna-dwelling chimpanzees, Pan troglodytes verus, at Mt. Assirik, Senegal. Primates 24: 154–173.

    Google Scholar 

  90. Vermeij, G. J. (1982). Unsuccessful predation and evolution. Am. Nat. 120: 701–720.

    Google Scholar 

  91. Wright, P.C. (1998). Impact of predation risk on the behaviour of Propithecus diadema edwardsi in the rain forest of Madagascar. Behaviour 135: 483–512.

    Google Scholar 

  92. Wright, P. C., Heckscher, S. K., and Dunham, A. E. (1997). Predation on Milne-Edward's sifaka (Propithecus diadema edwardsi) by the fossa (Cryptoprocta ferox) in the rain forest of southeastern Madagascar. Folia Primatol. 68: 34–43.

    Google Scholar 

  93. Zuberbühler, K., Noë , R., and Seyfarth, R. M. (1997). Diana monkey long-distance calls: Messages for conspecifics and predators. Anim. Behav. 53: 589–604.

    Google Scholar 

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  1. Jane Goodall Research Center and Department of Anthropology, University of Southern California, Los Angeles, California, 90089-0032

    Craig B. Stanford

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Stanford, C.B. Avoiding Predators: Expectations and Evidence in Primate Antipredator Behavior. International Journal of Primatology 23, 741–757 (2002). https://doi.org/10.1023/A:1015572814388

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  • predation
  • antipredator behavior
  • colobus
  • chimpanzees
  • sociality