International Journal of Primatology

, Volume 33, Issue 4, pp 860–871 | Cite as

Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack

  • Jacqueline S. Buhl
  • Bonn Aure
  • Angelina Ruiz-Lambides
  • Janis Gonzalez-Martinez
  • Michael L. Platt
  • Lauren J. N. Brent
Article

Abstract

Among animals that form social bonds, the death of a conspecific may be a significant social event, representing the loss of an ally and resulting in disruptions to the dominance hierarchy. Despite this potential biological importance, we have only limited knowledge of animals’ reactions to the death of a group member. This is particularly true of responses to dead adults, as most reports describe the responses of mothers to dead infants. Here, we describe in detail and provide video evidence of the behavioral responses of a group of free-ranging rhesus macaques (Macaca mulatta) immediately after the death of a mid-ranking adult male as a result of a fatal attack. High-ranking male members of the group, suspected to have carried out the attack, dragged and bit the dead body, exhibiting a rate of aggression 20 times greater than baseline levels. Lower-ranking individuals approached and inspected the body by looking closely, smelling, and grooming the fur. There was inconclusive evidence that these rhesus macaques found the death of a conspecific stressful: Levels of grooming between group members after the fatal attack were significantly higher than baseline levels, and higher than levels of grooming after nonfatal attacks. However, when grooming levels were adjusted based on the assumption that individuals positioned close to the body, i.e., those visible to researchers, were more likely to be engaged in grooming than those positioned farther away, this difference from baseline was no longer significant. The rate of self-directed behaviors after the fatal attack was also not different from baseline. Many of the behaviors we observed directed toward the body (aggression, inspection) have been previously reported in chimpanzees and geladas, and are similar to reactions sometimes displayed by humans. As such, this report represents a potentially valuable contribution the nascent field of nonhuman primate thanatology.

Keywords

Cognition Death Grooming Stress Thanatology 

Supplementary material

Supplementary Video

Responses by rhesus macaques to the body of a dead adult male member of their group. High-ranking individuals are seen directing aggression toward the body, while lower-ranking individuals are seen approaching, looking at, and grooming the body. Many group members are seen grooming one another, which may be a potential indicator of elevated stress levels. (MPG 53990 kb)

References

  1. Anderson, J. R. (2011). A primatological perspective on death. American Journal of Primatology, 73, 410–414.PubMedCrossRefGoogle Scholar
  2. Anderson, J. R., Gillies, A., & Lock, L. C. (2010). Pan thanatology. Current Biology, 20, R349–R351.PubMedCrossRefGoogle Scholar
  3. Boccia, M. L., Reite, M., & Laudenslager, M. (1989). On the physiology of grooming in a pigtail macaque. Physiology and Behavior, 45, 667–670.PubMedCrossRefGoogle Scholar
  4. Byrne, R. W., & Bates, L. A. (2010). Primate social cognition: Uniquely primate, uniquely social, or just unique? Neuron, 65, 815–830.PubMedCrossRefGoogle Scholar
  5. Cronin, K. A., van Leeuwen, E. J. C., Mulenga, I. C., & Bodamer, M. D. (2011). Behavioral response of a chimpanzee mother toward her dead infant. American Journal of Primatology, 73, 415–421.PubMedCrossRefGoogle Scholar
  6. Douglas-Hamilton, I., Bhalla, S., Wittemyer, G., & Vollrath, F. (2006). Behavioural reactions of elephants towards a dying and deceased matriarch. Applied Animal Behaviour Science, 100, 87–102.CrossRefGoogle Scholar
  7. Drews, C. (1993). The concept and definition of dominance in animal behaviour. Behaviour, 125, 283–313.CrossRefGoogle Scholar
  8. Engh, A. L., Beehner, J. C., Bergman, T. J., Whitten, P. L., Hoffmeier, R. R., Seyfarth, R. M., et al. (2006). Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proceedings of the Royal Society of London B: Biological Sciences, 273, 707–712.CrossRefGoogle Scholar
  9. Fashing, P. J., Nguyen, N., Barry, T. S., Goodale, C. B., Burke, R. J., Jones, S. C. Z., et al. (2010). Death among geladas (Theropithecus gelada): A broader perspective on mummified infants and primate thanatology. American Journal of Primatology, 71, 1–5.Google Scholar
  10. Gros-Louis, J., Perry, S., & Manson, J. H. (2003). Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys (Cebus capucinus). Primates, 44, 341–346.PubMedCrossRefGoogle Scholar
  11. Hadidian, J., & Bernstein, I. S. (1979). Female reproductive cycles and birth data from an Old World monkey colony. Primates, 20, 429–442.CrossRefGoogle Scholar
  12. Hatfield, E., Cacioppo, J. T., & Rapson, R. L. (1994). Emotional contagion. Cambridge: Cambridge University Press.Google Scholar
  13. Howard, D. F., & Tschinkel, W. R. (1976). Aspects of necrophoric behavior in red imported fire ant, Solenopsis invicta. Behaviour, 56, 157–180.CrossRefGoogle Scholar
  14. Irwin, M. R., Risch, S. C., Daniels, M., Bloom, E., & Weiner, H. (1987). Plasma-cortisol and immune function in bereavement. Psychosomatic Medicine, 49, 210–211.Google Scholar
  15. Martin, P., & Bateson, P. (1993). Measuring behaviour: An introductory guide (2nd ed.). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  16. McComb, K., Baker, L., & Moss, C. (2006). African elephants show high levels of interest in the skulls and ivory of their own species. Biology Letters, 2, 26–28.PubMedCrossRefGoogle Scholar
  17. Rawlings, R. G., & Kessler, M. J. (1986). The Cayo Santiago macaques: History, behavior & biology. Albany: State University of New York Press.Google Scholar
  18. Schino, G., Perretta, G., Taglioni, A. M., Monaco, V., & Troisi, A. (1996). Primate displacement activities as an ethopharmacological model of anxiety. Anxiety, 2, 186–191.PubMedCrossRefGoogle Scholar
  19. Semple, S., Higham, J. P., MacLarnon, A., Ross, C., & Lehmann, J. (2010). Comment on ‘Pan Thanatology’. Current Biology, http://www.cell.com/currentbiology/comments/S0960-9822(10)00145-4.
  20. Shutt, K., MacLarnon, A., Heistermann, M., & Semple, S. (2007). Grooming in Barbary macaques: Better to give than receive? Biology Letters, 3, 231–233.PubMedCrossRefGoogle Scholar
  21. Stewart, F. A., Piel, A. K., & O’Malley, R. C. (2012). Responses of chimpanzees to a recently dead community member at Gombe National Park, Tanzania. American Journal of Primatology, 74, 1–7.PubMedCrossRefGoogle Scholar
  22. Teleki, G. (1973). Group response to the accidental death of a chimpanzee in Gombe National Park, Tanzania. Folia Primatologica, 20, 81–94.CrossRefGoogle Scholar
  23. Valero, A., Schaffner, C. M., Vick, L. G., Aureli, F., & Ramos-Fernandez, G. (2006). Intragroup lethal aggression in wild spider monkeys. American Journal of Primatology, 68, 732–737.PubMedCrossRefGoogle Scholar
  24. Visscher, P. K. (1983). The honey bee way of death: necrophoric behavior in Apis mellifera colonies. Animal Behaviour, 31, 1070–1076.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Jacqueline S. Buhl
    • 1
  • Bonn Aure
    • 1
  • Angelina Ruiz-Lambides
    • 1
  • Janis Gonzalez-Martinez
    • 1
  • Michael L. Platt
    • 2
  • Lauren J. N. Brent
    • 3
  1. 1.Caribbean Primate Research CenterUniversity of Puerto RicoPunta SantiagoPuerto Rico
  2. 2.Duke Institute for Brain Sciences and Center for Cognitive Neuroscience and Departments of Neurobiology, Evolutionary Anthropology, and Psychology & NeuroscienceDuke UniversityDurhamUSA
  3. 3.Duke Institute for Brain Sciences and Center for Cognitive NeuroscienceDuke UniversityDurhamUSA

Personalised recommendations