International Journal of Primatology

, Volume 24, Issue 4, pp 759–796 | Cite as

Interspecific Interactions Between Cebus capucinus and Other Species: Data from Three Costa Rican Sites

  • Lisa M. Rose
  • Susan Perry
  • Melissa A. Panger
  • Katharine Jack
  • Joseph H. Manson
  • Julie Gros-Louis
  • Katherine C. Mackinnon
  • Erin Vogel


Capuchins exhibit considerable cross-site variation in domains such as foraging strategy, vocal communication and social interaction. We report interactions between white-faced capuchins (Cebus capucinus) and other species. We present comparative data for 11 groups from 3 sites in Costa Rica that are ecologically similar and geographically close, thus reducing the likelihood that differences are due solely to genetic or ecological differences. Our aim is to document both the range of variation and common elements across sites and situations. We also consider factors that contribute to the variation or consistency or both, including social learning, local ecology, and temperament. We consider 4 categories of allospecifics: (1) vertebrate prey, (2) potential predators, (3) feeding competitors, and (4) neutral species. Although we cannot rule out local differences in ecology, our data suggest that social learning may account for at least some cross-site differences in behavior toward allospecifics. Our strongest finding is that boldness, aggression and pugnacity are displayed consistently across sites, groups and circumstances, even in interactions with neutral species, which reflects a critical aspect of species-specific temperament in Cebus capucinus that has been evolutionarily developed and reinforced through highly opportunistic foraging, strong predator defense, and active hunting. We suggest directions for future research, particularly in regard to primate temperament as an evolved trait with consequences for fitness.

Cebus capucinus allospecifics predator-prey interactions social learning temperament 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Boesch, C. (1994). Chimpanzees-red colobus monkeys: A predator-prey system.Anim. Behav. 47: 1135-1148.Google Scholar
  2. Boinski, S. (1987). Birth synchrony in squirrel monkeys (Saimiri oerstedi): A strategy to reduce neonatal predation.Behav. Ecol. Sociobiol. 21: 393-400.Google Scholar
  3. Boinski, S. (1988). Use of a club by a wild white-faced capuchin (Cebus capucinus) to attack a venomous snake (Bothrops asper).Am. J. Primatol. 14: 177-179.Google Scholar
  4. Boinski, S. (1996). Vocal coordination of troop movement in squirrel monkeys (Saimiri oerstedi and S. sciureus) and white-faced capuchins (Cebus capucinus). In Norconk, M. A., Rosenberger, A. L., and Garber, P. A. (Eds.), Adaptive Radiations of Neotropical Primates, Plenum Press, New York, pp. 251-269.Google Scholar
  5. Boinski, S. (1999). Geographic variation in behavior of a primate taxon: Stress responses as a proximate mechanism in the evolution of social behavior. In Foster, S. A., and Endler, J. A. (Eds.), Geographic Variation in Behavior: Perspectives on Evolutionary Mechanisms, Oxford University Press, New York, pp. 95-120.Google Scholar
  6. Chapman, C. A. (1986). Boa constrictor predation and group response in white-faced Cebus monkeys.Biotropica 18: 171-172.Google Scholar
  7. Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican primates.Folia Primatol. 29: 90-105.Google Scholar
  8. Chapman, C. A. (1988). Patterns of foraging and range use by three species of Neotropical primates.Primates 29: 177-194.Google Scholar
  9. Chapman, C. A. (1989). Ecological constraints on group size in three species of Neotropical primates.Folia Primatol. 73: 1-9.Google Scholar
  10. Chapman, C. A., Chapman, L. J., and Glander, K. E. (1989). Primate populations in Northwestern Costa Rica: Potential for recovery.Primate. Conserv. 10: 37-44.Google Scholar
  11. Chapman, C. A., and Fedigan, L. M. (1990). Dietary differences between neighboring Cebus capucinus groups: Local traditions, food availability, or response to food profitability? Folia Primatol. 54: 177-186.Google Scholar
  12. Chapman, C. A., Wrangham, R., and Chapman, L. J. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups.Behav. Ecol. Sociobiol. 36: 59-70.Google Scholar
  13. Clarke, S., and Boinski, S. (1995). Temperament in nonhuman primates.Am. J. Primatol. 37: 103-135.Google Scholar
  14. Cook, M., and Mineka, S. (1990). Selective associations in the observational conditioning of fear in rhesus monkeys.J. Exp. Psych: Anim. Behav. Process. 16: 372-389.Google Scholar
  15. Custance, D., Whiten, A., and Fredman, T. (1999). Social learning of an artificial fruit task in capuchin monkeys (Cebus apella).J. Comp. Pyschol. 113: 13-23.Google Scholar
  16. Custance, D., Whiten, A., and Fredman, T. (2002). Social learning and primate reintroduction.Int. J. Primatol. 23: 479-499.Google Scholar
  17. Dolhinow, P. (1999). Play: A critical process in the developmental system. In Dolhinow, P., and Fuentes, A. (Eds.), The Nonhuman Primates, Mayfield, Mountain View, CA, pp. 231-236.Google Scholar
  18. Dolhinow, P., and Bishop, N. (1970). The development of motor skills and social relationships among primates through play.Minn. Symp. Child Psych. 4: 141-198.Google Scholar
  19. Fedigan, L. M. (1990). Vertebrate predation in Cebus capucinus: Meat eating in a Neotropical monkey.Folia Primatol. 54: 196-205.Google Scholar
  20. Fedigan, L. M. (1993). Sex differences and intersexual relations in adult white-faced capuchins, Cebus capucinus.Int. J. Primatol. 14: 853-877.Google Scholar
  21. Fedigan, L. M., and Jack, K. M. (2001). Neotropical primates in a regenerating Costa Rican dry forest: A comparison of howler and capuchin populations.Int. J. Primatol. 22: 689-713.Google Scholar
  22. Fedigan, L. M., Rose, L. M., and Avila, R. M. (1996). See how they grow: Tracking capuchin monkey populations in a regenerating Costa Rican dry forest. In Norconk, M. A., Rosenberger, A. L., and Garber, P. A. (Eds.), Adaptive Radiations of Neotropical Primates, Plenum Press, New York, pp. 289-307.Google Scholar
  23. Fedigan, L. M., Rose, L. M., and Avila, R. M. (1998). Growth of mantled howler groups in a regenerating Costa Rican dry forest.Int. J. Primatol. 19: 405-432.Google Scholar
  24. Fichtel, C., and Kappeler, P. M. (2002). Anti-predator behavior of group-living Malagasy primates: Mixed evidence for a referential alarm system.Behav. Ecol. Sociobiol. 51: 262-275.Google Scholar
  25. Fragaszy, D. M. (1990). Age and sex differences in the organization of behavior in wedge-capped capuchins, Cebus olivaceus.Behav. Ecol. 1: 81-94.Google Scholar
  26. Fragaszy, D. M., and Perry, S. (Eds.) (2003). The Biology of Traditions: Models and Evidence, Cambridge University Press, Cambridge, New York.Google Scholar
  27. Fragaszy, D. M., and Visalberghi, E. (1990). Social processes affecting the appearance of innovative behaviors in capuchin monkeys.Folia Primatol. 54: 155-165.Google Scholar
  28. Fragaszy, D. M., Visalberghi, E., and Robinson, J. G. (1990). Variability and adaptability in the genus Cebus.Folia Primatol. 54: 114-118.Google Scholar
  29. Frankie, G. W., Baker, H. G., and Opler, P. A. (1974). Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica.J. Ecology 62: 881-919.Google Scholar
  30. Frankie, G. W., Vinston, S. B., Newstrom, L. E., and Barthell, J. F. (1988). Nest site and habitat preferences of Cintris bees in the Costa Rican dry forest.Biotropica 20: 301-310.Google Scholar
  31. Galef, B. G., Mittermeier, R. A., and Bailey, R. C. (1978). Predation by the tayra (Eira barbara).J. Mammal. 57: 760-761.Google Scholar
  32. Gautier-Hion, A.; Quris, A., and Gautier, J. P. (1983). Monospecific vs. polyspecific life: A comparative study of foraging and antipredator tactics in a community of Cercopithecus monkeys.Behav. Ecol. Sociobiol. 12: 325-335.Google Scholar
  33. Gosling, S. D., and John, O. P. (1999). Personality dimensions in nonhuman animals: A cross-species review.Curr. Dir. Pysch. Sci. 8: 69-75.Google Scholar
  34. Gros-Louis, J. (2002). Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus).Am. J. Primatol. 57: 189-202.Google Scholar
  35. Hill, K., Kaplan, H., Hawkes, K., and Hurtado, A. M. (1985). Men's time allocation to subsistence work among the Ache of Eastern Paraguay.Hum. Ecol. 13: 29-47.Google Scholar
  36. Jack, K. (2001). Effect of male emigration on the vigilance behavior of coresident males in white-faced capuchins (Cebus capucinus).Int. J. Primatol. 22: 715-732.Google Scholar
  37. Janson, C. H., and Boinski, S. (1992). Morphological and behavioral adaptations for foraging in generalist primates: The case of the Cebines.Am. J. Primatol. 88: 483-498.Google Scholar
  38. Janzen, D. H. (1983). Costa Rican Natural History, University of Chicago Press, Chicago.Google Scholar
  39. Jolly, A. (1985). The Evolution of Primate Behaviour, 2nd edn., MacMillan, New York.Google Scholar
  40. Karli, P. (1989). Is the concept of “personality” relevant to the study of animal aggression? Eur. J. Pers. 3: 139-148.Google Scholar
  41. MacKinnon, K. C. (2002). Social Development of White-Faced Capuchin Monkeys (Cebus capucinus) in Costa Rica: An Examination of Social Interactions Between Immatures and Adult Males, PhD Dissertation, University of California, Berkeley.Google Scholar
  42. Manson, J. H., and Perry, S. (2000). Correlates of self-directed behavior in wild white-faced capuchins.Ethology 106: 301-317.Google Scholar
  43. Manson, J. H., Rose, L. M., Perry, S., and Gros-Louis, J. (1999). Dynamics of female-female relationships in wild Cebus capucinus: Data from two Costa Rican sites.Int. J. Primatol. 20: 679-706.Google Scholar
  44. Massey, J. (1987). A population survey of Alouatta palliata, Cebus capucinus and Ateles geoffroyi at Palo Verde, Costa Rica.Rev. Biol. Tropicale 35: 345-347.Google Scholar
  45. Olmos, F. (1994). Jaguar predation on muriqui Brachyteles arachnoides.Neotrop. Prim. 2: 16.Google Scholar
  46. Oppenheimer, J. R. (1982). Cebus capucinus: Home range, population dynamics, and interspecific relationships. In Leigh, E. G., Rand, A. S., and Windsor, D. M. (Eds.), The Ecology of a Tropical Forest: Seasonal Rhythms and Long-Term Changes, Smithsonian Institution Press, Washington, DC, pp. 253-270.Google Scholar
  47. Panger, M. A. (1997). Hand Preference and Object Use in Free-Ranging White-Faced Capuchins (Cebus capucinus) in Costa Rica, PhD Thesis, University of California, Berkeley.Google Scholar
  48. Panger, M. A. (1998). Object use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica.Am. J. Phys. Anthropol. 106: 311-321.Google Scholar
  49. Panger, M. A. (1999). Capuchin object manipulation. In Dolhinow, P., and Fuentes, A. (eds). The Nonhuman Primates, Mayfield, Mountain View, CA, pp. 115-120.Google Scholar
  50. Panger, M. A., Perry, S., Rose, L. M., Gros-Louis, J., Vogel, E., MacKinnon, K. C., and Baker, M. (2002). Cross-site differences in the foraging behavior of white-faced capuchins (Cebus capucinus).Am. J. Phys. Anthropol. 119: 52-66.Google Scholar
  51. Peetz, A., Norconk, M. A., and Kinzey, W. G. (1992). Predation by jaguar on howler monkeys (Alouatta seniculus) in Venezuela.Am. J. Primatol. 28: 223-228.Google Scholar
  52. Perry, S. (1995). Social Relationships in Wild White-Faced Capuchin Monkeys, Cebus capucinus, PhD Dissertation, University of Michigan.Google Scholar
  53. Perry, S. (1996a). Intergroup encounters in white-faced capuchin monkeys (Cebus capucinus).Int. J. Primatol. 17: 309-330.Google Scholar
  54. Perry, S. (1996b). Female-female social relationships in wild white-faced capuchin monkeys (Cebus capucinus).Am. J. Primatol. 40: 167-182.Google Scholar
  55. Perry, S. (1997). Male-female social relationships in wild white-faced capuchin monkeys (Cebus capucinus).Behaviour 134: 477-510.Google Scholar
  56. Perry, S. (1998). Male-male social relationships in wild white-faced capuchins, Cebus capucinus.Behaviour 135: 1-34.Google Scholar
  57. Perry, S. (2003). Coalitionary aggression in white-faced capuchins. In de Waal, F. B. M., and Tyack, P. (Eds.), Animal Social Complexity: Intelligence, Culture, and Individualized Societies, Harvard University Press, pp. 111-114.Google Scholar
  58. Perry, S., Baker, M., Fedigan, L. M., Gros-Louis, J., Jack, K., MacKinnon, K. C., Manson, J. H., Panger, M., Pyle, K., and Rose, L. M. (2003). Social conventions in wild white-faced capuchins: Evidence for traditions in a Neotropical primate.Curr. Anthropol. 44: 241-268.Google Scholar
  59. Perry, S., Panger, M., Rose, L., Baker, M., Gros-Louis, J., Jack, K., MacKinnon, K. C., Manson, J. H., Fedigan, K. and Pyle, K. (2003). Traditions in wild white-faced capuchins. In Fragaszy, D. M., and Perry, S. (Eds.), The Biology of Traditions: Models and Evidence, Cambridge University Press, Cambridge, New York, pp. 391-425.Google Scholar
  60. Porter, L. M. (2001). Dietary differences among sympatric Callitrichinae in Northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. Labiatus.Int. J. Primatol. 22: 961-992.Google Scholar
  61. Redford, K. H., and Robinson, J. G. (1991). Subsistence and commercial uses of wildlife in Latin America. In Robinson, J. G. (ed.), Neotropical Wildlife Use and Conservation, University of Chicago Press, Chicago pp. 6-23.Google Scholar
  62. Rose, L. M. (1994a). Benefits and costs of resident males to females in white-faced capuchins, Cebus capucinus.Am. J. Primatol. 32: 235-248.Google Scholar
  63. Rose, L. M. (1994b). Sex differences in the diet and foraging behavior in white-faced capuchins, Cebus capucinus.Int. J. Primatol. 15: 63-82.Google Scholar
  64. Rose, L. M. (1997). Vertebrate predation and food-sharing in Cebus and Pan. Int. J. Primatol. 18: 727-765. aiRose, L. M. (1998). Behavioral Ecology of White-Faced Capuchins (Cebus capucinus) in Costa Rica, PhD Dissertation, Washington University, St. Louis, MO.Google Scholar
  65. Rose, L. M. (2001). Meat and the early human diet: Insights from Neotropical primate studies. In Stanford, C. B., and Bunn, H. (Eds.), Meat-Eating and Human Evolution, Oxford University Press, Oxford, pp. 141-158Google Scholar
  66. Rose, L. M., and Fedigan, L. M. (1995). Vigilance in white-faced capuchins, Cebus capucinus.Anim. Behav. 49: 63-70.Google Scholar
  67. Sauther, M. L. (1989). Antipredator behavior in troops of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar.Int. J. Primatol. 10: 495-606.Google Scholar
  68. Seyfarth, R. M., Cheney, D. L., and Marler, P. (1980). Monkey response to three different alarm calls: Evidence of predator classification and semantic communication.Science 210: 810-813.Google Scholar
  69. Sherman, P. T. (1991). Harpy eagle predation on a red howler monkey.Folia Primatol. 56: 53-65.Google Scholar
  70. Smith, E. O. (1978). A historical view on the study of play: Statement of the problem. In Smith, E. O. (ed.), Social Play in Primates, Academic Press, New York, pp. 1-32.Google Scholar
  71. Stanford, C. B. (1998). Chimpanzee and Red Colobus: The Ecology of Predator and Prey, Harvard University Press, Cambridge, MA.Google Scholar
  72. Stanford, C. B. (2002). Avoiding predators: Expectations and evidence in primate antipredator behavior.Int. J. Primatol. 23: 741-757.Google Scholar
  73. Stevenson-Hinde, J., and Zunz, M. (1978). Subjective assessment of individual rhesus monkeys.Primates 21: 66-68.Google Scholar
  74. Taylor, P. D., and Jonker, L. B. (1978). Evolutionarily stable strategies and game dynamics.Math. BioSci. 40: 145-156.Google Scholar
  75. Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology, Princeton University Press, Princeton.Google Scholar
  76. Tutin, C. E. G., McGrew, W. C., and Baldwin, P. (1981). Responses of wild chimpanzees to potential predators. In Chiarelli, A. B., and Corruccini, R. S. (Eds.), Primate Behavior and Sociobiology, Springer-Verlag, Berlin, pp. 136-141.Google Scholar
  77. Visalberghi, E., and Addessi, E. (2000). Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys.Anim. Behav. 60: 69-76.Google Scholar
  78. Vitale, A F., Visalberghi, E., and de Lillo, C. (1991). Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella).Int. J. Primatol. 12: 277-286.Google Scholar
  79. Wahunga, G. M. (1998). Diet and habitat overlap in two sympatric primate species, the Tana River crested mangabey Cercopithecus galeritus and yellow baboon, Papio cynocephalus.African J. Ecol. 36: 159-173.Google Scholar
  80. Watts, D. P., and Mitani, J. C. (2002). Hunting behavior of chimpanzees at Ngogo, Kibale National Park, Uganda.Int. J. Primatol. 23: 1-28Google Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • Lisa M. Rose
    • 1
  • Susan Perry
    • 1
  • Melissa A. Panger
    • 1
  • Katharine Jack
    • 2
  • Joseph H. Manson
    • 1
  • Julie Gros-Louis
    • 2
  • Katherine C. Mackinnon
    • 3
  • Erin Vogel
    • 4
  1. 1.Department AnthropologyUniversity of British ColumbiaVancouver, B.C.
  2. 2.Department AnthropologyAppalachian State UniversityBoone
  3. 3.Department Sociology and Criminal JusticeSt. Louis UniversitySt. Louis
  4. 4.Department Ecology and EvolutionState University of New YorkStony Brook

Personalised recommendations