Coping with Acute Crowding by Cebus apella

Traditionally, scientists believed that crowded housing conditions increased aggression in animals. Recent research on captive primates fails to support a linear relationship between population density and aggressive behavior. Our study is the first to investigate the effects of acute crowding on a New World primate. We observed brown capuchins (Cebus apella) under 2 different spatial conditions: a control that offered the full indoor space in the enclosure and a short-term experimental condition that restricted the capuchins to approximately half the amount of space of the control condition. We compared rates of self-grooming, aggression, contact sitting, social grooming, and play between both conditions. We conducted a mixed factorial ANOVA at the individual level while taking subject sex and age class into account. Intense aggression, play, and social grooming decreased significantly in crowded conditions, suggesting that capuchins avoid social encounters if spatially confined. Their strategy for coping with acute crowding via a decrease in all forms of social behavior is intermediate between chimpanzee and macaque strategies in similar experiments. The only behavior to increase under crowding was a nonsocial, self-directed behavior with the potential of reducing arousal: self-grooming.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

REFERENCES

  1. Alexander, B. K., and Roth, E. M. (1971). The effects of acute crowding on aggressive behavior of Japanese monkeys. Behaviour 39: 73–90.

    PubMed  CAS  Google Scholar 

  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour 49: 227–267.

    PubMed  CAS  Google Scholar 

  3. Andrew, R. (1965). The origins of facial expressions. Sci. Am. 213: 88–94.

    PubMed  CAS  Article  Google Scholar 

  4. Aureli, F., and de Waal, F. B. M. (1997). Inhibition of social behavior in chimpanzee under high-density conditions. Am. J. Primatol. 41: 213–228.

    PubMed  CAS  Article  Google Scholar 

  5. Aureli, F., Preston, S. D., and de Waal, F. B. M. (1999). Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): A pilot study. J. Comp. Psychol. 113: 59–65.

    PubMed  CAS  Article  Google Scholar 

  6. Aureli, F., van Panthaleon van Eck, C. J., and Veenema, H. C. (1995). Long-tailed macaques avoid conflicts during short-term crowding. Agress. Behav. 21: 113–122.

    Google Scholar 

  7. Bercovitch, F. B., and Lebron, M. R. (1991). Impact of artificial fissioning and social networks on levels of aggression and affiliation in primates. Agress. Behav. 17: 17–25.

    Google Scholar 

  8. Boesch, C. (1994). Cooperative hunting in wild chimpanzees. Anim. Behav. 48: 653–667.

    Article  Google Scholar 

  9. Boesch, C. (2002). Cooperative hunting roles among Tai chimpanzees. Hum. Nat. 13: 27–46.

    Google Scholar 

  10. Boesch, C., and Boesch-Achermann, H. (2000). The Chimpanzees of the Tai Forest: Behavioral Ecology and Evolution. Oxford University Press, Oxford.

    Google Scholar 

  11. Calhoun, J. B. (1962). Population density and social pathology. Sci. Am. 206: 139–148.

    PubMed  CAS  Google Scholar 

  12. de Waal, F. B. M. (1986). The integration of dominance and social bonding in primates. Quart. Rev. Biol. 61: 459–479.

    PubMed  CAS  Article  Google Scholar 

  13. de Waal, F. B. M. (1989a). The myth of a simple relation between space and aggression in captive primates. Zoo Biol. Suppl. 1: 141–148.

    Article  Google Scholar 

  14. de Waal, F. B. M. (1989b). Food sharing and reciprocal obligations among chimpanzees. J. Hum. Evol. 18: 433–459.

    Article  Google Scholar 

  15. de Waal, F. B. M. (1997). Food transfers through mesh in brown capuchins. J. Comp. Psychol. 111: 370–378.

    PubMed  CAS  Article  Google Scholar 

  16. de Waal, F. B. M., Aureli, F., and Judge, P. G. (2000). Coping with crowding. Sci. Am. 282: 76–81.

    PubMed  CAS  Article  Google Scholar 

  17. de Waal, F. B. M., and Luttrell, L. M. (1985). The formal hierarchy of rhesus macaques: An investigation of the bared-teeth display. Am. J. Primatol. 9: 73–85.

    Article  Google Scholar 

  18. Eaton, G. G., Modahl, K. B., and Johnson, D. F. (1981). Aggressive behavior in a confined troop of Japanese macaques: Effects of density, season, and gender. Aggress. Behav. 7: 145–164.

    Google Scholar 

  19. Elton, R. H., and Anderson, B. V. (1977). The social behavior of a group of baboons (Papio anubis) under artificial crowding. Primates 18: 225–234.

    Article  Google Scholar 

  20. Fedigan, L. M. (1990). Vertebrate predation in Cebus capucinus: Meat eating in a neotropical monkey. Folia Primatol. 54: 196–205.

    PubMed  CAS  Article  Google Scholar 

  21. Fragaszy, D. M., Fedigan, L., and Visalberghi, E. (2004). The Complete Capuchins: The Biology of the Genus Cebus. Cambridge University Press, NY.

    Google Scholar 

  22. Freedman, J. L., Levy, A. S., Buchanan, R. W., and Price, J. (1972). Crowding and human aggressiveness. J. Exp. Soc. Psychol. 8: 528–548.

    Article  Google Scholar 

  23. Freese, C. H., and Oppenheimer, J. R. (1981). The capuchin monkeys, genus Cebus. In Coimbra-Filho, A. F., and Mittermeier, R. A. (eds.), Ecology and Behavior of Neotropical Primates. Academia Brasileira de Ciencias, Rio de Janeiro, pp. 331–390.

    Google Scholar 

  24. Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Belknap Press, Cambridge, MA.

    Google Scholar 

  25. Hall, C. L., and Fedigan, L. M. (1997). Spatial benefits afforded by high rank in white-faced capuchins. Anim. Behav. 53: 1069–1082.

    Article  Google Scholar 

  26. Judge, P. G. (2000). Coping with crowded conditions. In Aureli, F., and de Waal, F. B. M. (eds.), Natural Conflict Resolution. University of California Press, Berkeley, pp. 129–154.

    Google Scholar 

  27. Judge, P. G., and de Waal, F. B. M. (1993). Conflict avoidance among rhesus monkeys: Coping with short-term crowding. Anim. Behav. 46: 221–232.

    Article  Google Scholar 

  28. Judge, P. G., and de Waal, F. B. M. (1997). Rhesus monkey behaviour under diverse population densities: Coping with long-term crowding. Anim. Behav. 54: 643–662.

    PubMed  Article  Google Scholar 

  29. Kauffman, L. M., Ehmke, E. E., and Boinski, S. (2004). Increased male-male cooperation among brown capuchin monkeys (Cebus apella) in Suriname. Folia Primat. 75: 287–288.

    Google Scholar 

  30. Lancaster, J. B. (1986). Primate social behavior and ostracism. Ethol. Sociobiol. 7: 215–225.

    Article  Google Scholar 

  31. Maestripieri, D., Schino, G., Aureli, F., and Troisi, A. (1992). A modest proposal: Displacement activities as an indicator of emotions in primates. Anim. Behav. 44: 967–979.

    Article  Google Scholar 

  32. Marascuilo, L. A., and Serlin, R. C. (1988). Statistical Methods for the Social and Behavioral Sciences. Witt, Freeman, New York.

    Google Scholar 

  33. Maxim, P. E. (1982). Contexts and messages in macaque social communication. Am. J. Primatol. 2: 63–85.

    Article  Google Scholar 

  34. Mendres, K. A., and de Waal, F. B. M. (2000). Capuchins do cooperate: The advantage of an intuitive task. Anim. Behav. 60: 523–529.

    PubMed  Article  Google Scholar 

  35. Nieuwenhuijsen, K., and de Waal, F. B. M. (1982). Effects of spatial crowding on social behavior in a chimpanzee colony. Zoo Biol. 1: 5–28.

    Article  Google Scholar 

  36. O’Brien, T. G. (1993a). Asymmetries in grooming interactions between juvenile and adult female wedge-capped capuchin monkeys. Anim. Behav. 46: 929–938.

    Article  Google Scholar 

  37. O’Brien, T. G. (1993b). Allogrooming behaviour among adult female wedge-capped capuchin monkeys. Anim. Behav. 46: 499–510.

    Article  Google Scholar 

  38. Ottoni, E. B., and Mannu, M. (2001). Semifree-ranging tufted capuchins (Cebus apella) spontaneously use tools to crack open nuts. Int. J. Primatol. 22: 347–358.

    Article  Google Scholar 

  39. Perry, S. (1996). Intergroup encounters in wild white-faced capuchins (Cebus capucinus). Int. J. Primatol. 17: 309–330.

    Google Scholar 

  40. Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., MacKinnon, K. C., Manson, J. H., Panger, M., Pyle, K., and Rose, L. (2003). Social conventions in wild white-faced capuchin monkeys. Curr. Anthropol. 44: 241–268.

    Article  Google Scholar 

  41. Perry, S., and Rose, L. (1994). Begging and transfer of coati meat by white-faced capuchin monkeys. Cebus capucinus. Primates 35: 409–415.

    Article  Google Scholar 

  42. Preuschoft, S., and van Schaik, C. P. (2000). Dominance and communication: Conflict management in various social settings. In Aureli, F., and de Waal, F. B. M. (eds.), Natural Conflict Resolution. University of California Press, Berkeley, pp. 77–105.

    Google Scholar 

  43. Rose, L. M. (1997). Vertebrate predation and food sharing in Cebus and Pan. Int. J. Primatol. 18: 727–765.

    Article  Google Scholar 

  44. Seyfarth, R. M., and Cheney, D. L. (1988). Empirical tests of reciprocity theory: Problems in assessment. Ethol. Sociobiol. 9: 181–187.

    Article  Google Scholar 

  45. Silk, J. B. (1982). Altruism among female Macaca radiata: Explanations and analysis of patterns of grooming and coalition formation. Behav 79: 162–188.

    Google Scholar 

  46. Taylor, S. E. (2002). The Tending Instinct: How Nurturing Is Essential for Who We Are and How We Live. Times Books, New York.

    Google Scholar 

  47. Terry, R. L. (1970). Primate grooming as a tension reduction mechanism. J. Psychol. 76: 129–136.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  49. Verbeek, P., and de Waal, F. B. M. (1997). Post-conflict behavior of captive brown capuchins in the presence and absence of attractive food. Int. J. Primatol. 18: 703–725.

    Article  Google Scholar 

  50. Watts, D. P., and Mitani, J. C. (2001). Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138: 299–327.

    Article  Google Scholar 

  51. Westergaard, G. C., Lundquist, A. L., Kuhn, H. E., and Suomi, S. J. (1997). Ant-gathering with tools by captive tufted capuchins (Cebus apella). Int. J. Primatol. 18: 95–103.

    Article  Google Scholar 

  52. Westergaard, G. C., and Suomi, S. J. (1994). Hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella). Am. J. Primatol. 32: 171–176.

    Article  Google Scholar 

  53. Westergaard, G. C., and Suomi, S. J. (1997). Transfer of tools and food between groups of tufted capuchins (Cebus apella). Am. J. Primatol. 43: 33–41.

    PubMed  CAS  Article  Google Scholar 

  54. Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama Y., Tutin, C. E. G., Wrangham, R. W., and Boesch, C. (1999). Culture in chimpanzees. Nature 399: 682–685.

    PubMed  CAS  Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

A grant from the National Science Foundation (IBN-0077706) to Frans de Waal and a grant from the National Institutes of Health (RR-00165) to the Yerkes National Primate Center supported the research. We thank Marietta Dindo, Marisa Hall, and Michelle Berger for assistance with the experiments and manuscript preparation and Nancy Bliwise for her help with statistical analyses. We also thank the animal care and veterinary staff at the Yerkes Primate Center. The facility is fully accredited by the American Association for the Accreditation of Laboratory Animal Care.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Megan L. van Wolkenten.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

van Wolkenten, M.L., Davis, J.M., Gong, M.L. et al. Coping with Acute Crowding by Cebus apella . Int J Primatol 27, 1241–1256 (2006). https://doi.org/10.1007/s10764-006-9070-z

Download citation

KEY WORDS:

  • aggression
  • Cebus apella
  • coping model
  • crowding
  • husbandry