Behavioral responses to injury and death in wild Barbary macaques (Macaca sylvanus)

Abstract

The wounding or death of a conspecific has been shown to elicit varied behavioral responses throughout thanatology. Recently, a number of reports have presented contentious evidence of epimeletic behavior towards the dying and dead among non-human animals, a behavioral trait previously considered uniquely human. Here, we report on the behavioral responses of Barbary macaques, a social, non-human primate, to the deaths of four group members (one high-ranking adult female, one high-ranking adult male, one juvenile male, and one female infant), all caused by road traffic accidents. Responses appeared to vary based on the nature of the death (protracted or instant) and the age class of the deceased. Responses included several behaviors with potential adaptive explanations or consequences. These included exploration, caretaking (guarding, carrying, and grooming), and proximity to wounded individuals or corpses, and immediate as well as longer-lasting distress behaviors from other group members following death, all of which have been reported in other non-human primate species. These observations add to a growing body of comparative evolutionary analysis of primate thanatology and help to highlight the multifaceted impacts of human-induced fatalities on an endangered and socially complex primate.

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References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    CAS  Article  PubMed  Google Scholar 

  2. Anderson JR (2011) A primatological perspective on death. Am J Primatol 73:410–414

    Article  PubMed  Google Scholar 

  3. Anderson JR, Gillies A, Lock LC (2010) Pan thanatology. Curr Biol 20:R349–R351

    CAS  Article  PubMed  Google Scholar 

  4. Appleby R, Smith B, Jones D (2013) Observations of a free-ranging adult female dingo (Canis dingo) and litter mates’ responses to the death of a pup. Behav Process 96:42–46

    Article  Google Scholar 

  5. Bercovitch FB (2012) Giraffe cow reaction to the death of her newborn calf. Afr J Ecol 51:376–379

    Article  Google Scholar 

  6. Bezerra BM, Keasey MP, Schiel N, da Silva Souto A (2014) Responses towards a dying adult group member in a New World monkey. Primates 55:185–188

    Article  PubMed  Google Scholar 

  7. Biro D, Humle T, Koops K, Sousa C, Hayashi M, Matsuzawa T (2010) Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Curr Biol 20:R351–R352

    CAS  Article  PubMed  Google Scholar 

  8. Boesch C (1991) The effects of leopard predation on grouping patterns in forest chimpanzees. Behavior 117:220–242

    Article  Google Scholar 

  9. Buhl JS, Aure B, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML, Brent LJN (2012) Response of Rhesus macaques (Macaca mulatta) to the body of a group member that died from a fatal attack. Int J Primatol 33:860–871

    Article  PubMed  PubMed Central  Google Scholar 

  10. Counts DR, Counts DA (1991) Coping with the final tragedy: cultural variation in dying and grieving. Baywood Publishing Company Inc, Amityville

    Google Scholar 

  11. Cronin KA, van Leeuwen EJC, Mulenga IC, Bodamer MD (2011) Behavioral response of a chimpanzee mother toward her dead infant. Int J Primatol 73:415–421

    Article  Google Scholar 

  12. Davenport LC (2010) Aid to a declining matriarch in the Giant Otter (Pteronura brasiliensis). PLoS One 5:e11385. doi:10.1371/journal.pone.0011385

    Article  PubMed  PubMed Central  Google Scholar 

  13. David HA (1987) Ranking from unbalanced paired-comparison data. Biometrika 74:432–436

    Article  Google Scholar 

  14. Deag JM (1980) Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis. Behaviour 75:54–80

    Article  Google Scholar 

  15. Dellatore DF, Waitt CD, Foitova I (2009) Two cases of mother-infant cannibalism orang-utans. Primates 50:277–281

    Article  PubMed  Google Scholar 

  16. Douglas-Hamilton I, Bhalla S, Wittemyer G, Vollrath F (2006) Behavioural reactions of elephants towards a dying and deceased matriarch. Appl Anim Behav Sci 100:87–102

    Article  Google Scholar 

  17. Fashing PJ, Nguyen N (2011) Behavior toward the dying, diseased, or disabled among animals and its relevance to paleopathology. Int J Paleopathol 1:128–129

    Article  Google Scholar 

  18. Fashing PJ, Nguyen N, Barry TS, Goodale CB, Burke RJ, Jones SC, Kerby JT, Lee LM, Nurmi NO, Venkataraman VV (2011) Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology. Am J Primatol 73:405–409

    Article  PubMed  Google Scholar 

  19. Fooden J (2007) Systematic review of the Barbary Macaque, Macaca Sylvanus (Linnaeus, 1758). Fieldiana Zool 113:1–60

    Article  Google Scholar 

  20. Hirshfield MF, Tinkle DW (1975) Natural selection and the evolution of reproductive effort. Proc Natl Acad Sci USA 72:2227–2231

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Hrdy SB (1999) Mother nature: a history of mothers, infants and natural selection. Pantheon Books, New York, p 752

    Google Scholar 

  22. Johnson ET, Snyder-Mackler N, Beehner JC, Bergman TJ (2014) Kinship and dominance rank influence the strength of social bonds in female geladas (Theropithecus gelada). Int J Primat 35:288–304

    Article  Google Scholar 

  23. Kaburu SK, MacLarnon A, Majolo B, Qarro M, Semple S (2012) Dominance rank and self-scratching among wild female Barbary macaques (Macaca sylvanus). Afr Zool 47:74–79

    Article  Google Scholar 

  24. Li T, Ren B, Li D, Zhang Y, Li M (2012) Maternal responses to dead infants in Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Nature Reserve, Yunnan, China. Primates 53:127–132

    Article  PubMed  Google Scholar 

  25. Majolo B, McFarland R (2009) Self-suckling in Barbary macaque (Macaca sylvanus) mothers before and after the death of their infant. Am J Primatol 140:381–383

    Google Scholar 

  26. Merz E (1978) Male-male interactions with dead infants in Macaca sylvanus. Primates 19:749–754

    Article  Google Scholar 

  27. Park KJ, Sohn H, An YR, Moon DY, Choi SG, An DH (2013) An unusual case of care-giving behavior in wild long-beaked common dolphins (Delphinus capensis) in the East Sea. Mar Mam Sci 29:E508–E514

    Google Scholar 

  28. Small MF (1990) Alloparental behavior in Barbary macaques, Macaca sylvanus. Anim Behav 39:297–306

    Article  Google Scholar 

  29. Stewart FA, Piel AK, O‘Malley RC (2012) Responses of chimpanzees to a recently dead community member at Gombe National Park, Tanzania. Am J Primatol 74:1–7

    Article  PubMed  Google Scholar 

  30. Sugiyama Y, Kurita H, Matsui T, Kimoto S, Shimomura T (2009) Carrying of dead infants by Japanese macaque (Macaca fuscata) mothers. Anthropol Sci 117:113–119

    Article  Google Scholar 

  31. Van Lavieren E, Wich S (2010) Decline of the endangered Barbary macaque Macaca sylvanus in the cedar forest of the Middle Atlas Mountains, Morocco. Oryx 44:133–138

    Article  Google Scholar 

  32. Warren Y, Williamson (2004) Transport of dead infant mountain gorillas by mothers and unrelated females. Zoo Biol 23:375–378

    Article  Google Scholar 

  33. Young C, Majolo B, Schülke O, Ostner J (2014) Male social bonds and rank predict supporter selection in cooperative aggression in wild Barbary macaques. Anim Behav 95:23–32

    Article  Google Scholar 

Download references

Acknowledgments

We thank Ifrane National Park, the Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification, Ecole Nationale Forestiere d’Ingeniuers and Institut Scientifique de Rabat for research permission and facilitation. We thank Melanie LaCava, Kevin Remeuf, Selma El Fassi-Fihri and Els van Laverien for their contribution to incident reporting, photography and filming. We thank Alice Marks and Selma El Fassi-Fihri for efforts collecting data on the dominance hierarchies. Finally, we thank Dr Caroline Ross, Dr Julia Lehmann and Prof Ann MacLarnon for their comments in the writing of this manuscript.

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Correspondence to Patrick J. Tkaczynski.

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L. A. D Campbell and P. J. Tkaczynski equally contributed to this work.

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Campbell, L.A.D., Tkaczynski, P.J., Mouna, M. et al. Behavioral responses to injury and death in wild Barbary macaques (Macaca sylvanus). Primates 57, 309–315 (2016). https://doi.org/10.1007/s10329-016-0540-4

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Keywords

  • Thanatology
  • Barbary macaque
  • Epimeletic behavior