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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Anderson JR (2011) A primatological perspective on death. Am J Primatol 73:410–414
Anderson JR, Gillies A, Lock LC (2010) Pan thanatology. Curr Biol 20:R349–R351
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
Bercovitch FB (2012) Giraffe cow reaction to the death of her newborn calf. Afr J Ecol 51:376–379
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
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
Boesch C (1991) The effects of leopard predation on grouping patterns in forest chimpanzees. Behavior 117:220–242
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
Counts DR, Counts DA (1991) Coping with the final tragedy: cultural variation in dying and grieving. Baywood Publishing Company Inc, Amityville
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
Davenport LC (2010) Aid to a declining matriarch in the Giant Otter (Pteronura brasiliensis). PLoS One 5:e11385. doi:10.1371/journal.pone.0011385
David HA (1987) Ranking from unbalanced paired-comparison data. Biometrika 74:432–436
Deag JM (1980) Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis. Behaviour 75:54–80
Dellatore DF, Waitt CD, Foitova I (2009) Two cases of mother-infant cannibalism orang-utans. Primates 50:277–281
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
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
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
Fooden J (2007) Systematic review of the Barbary Macaque, Macaca Sylvanus (Linnaeus, 1758). Fieldiana Zool 113:1–60
Hirshfield MF, Tinkle DW (1975) Natural selection and the evolution of reproductive effort. Proc Natl Acad Sci USA 72:2227–2231
Hrdy SB (1999) Mother nature: a history of mothers, infants and natural selection. Pantheon Books, New York, p 752
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
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
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
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
Merz E (1978) Male-male interactions with dead infants in Macaca sylvanus. Primates 19:749–754
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
Small MF (1990) Alloparental behavior in Barbary macaques, Macaca sylvanus. Anim Behav 39:297–306
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
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
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
Warren Y, Williamson (2004) Transport of dead infant mountain gorillas by mothers and unrelated females. Zoo Biol 23:375–378
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
L. A. D Campbell and P. J. Tkaczynski equally contributed to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary material 2 (MOV 42.5 mb)
Supplementary material 3 (MOV 26.2 mb)
Supplementary material 4 (MP4 41567 kb)
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-016-0540-4