Abstract
The observation of specific reactions by animals to dead conspecifics raises questions about their capacity to understand death. We describe the behavior of a captive group of tufted capuchins in the hours following the death of an adult female. The behavior of 12 subjects was recorded over a 5-h period. Most group members displayed exploratory behaviors toward the corpse, peering at it, smelling, touching, lifting or pulling it at least once. Interactions with the corpse were particularly frequent in the first hour, then decreased in the following hours. The relatives of the deceased female were the most involved individuals, and her daughter spent more time near her body than the other members of the group. Rates of interaction with the body were especially high in subadult individuals. Most of the behaviors directed to the body of the deceased individual appeared to be investigative.
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References
Anderson JR (2018) Chimpanzees and death. Phil Trans R Soc B 373:20170257. https://doi.org/10.1098/rstb.2017.0257
Anderson JR, Gillies A, Lock LC (2010) Pan thanatology. Curr Biol 20:R349–R351. https://doi.org/10.1016/j.cub.2010.02.010
Bezzera BM, Keasey MP, Sciel N, Da Silva Souto A (2014) Responses towards a dying adult group member in a wild New World monkey. Primates 55:185–188. https://doi.org/10.1007/s10329-014-0412-8
Biro D, Humle T, Koops K, Souza C, Hayashi M, Matsuzawa T (2010) Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Curr Biol 20:R351–R352. https://doi.org/10.1016/j.cub.2010.02.031
Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Tai forest: behavioural ecology and evolution. Oxford University Press, New York
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. https://doi.org/10.1007/s10764-012-9624-1
Campbell LAD, Tkaczynski PJ, Mouna M, Qarro M, Waterman J, Majolo B (2016) Behavioral responses to injury and death in wild Barbary macaques (Macaca sylvanus). Primates 57:309–315. https://doi.org/10.1007/s10329-016-0540-4
Cronin KA, van Leeuwen EJC, Mulenga IC, Bodamer MD (2011) Behavioral response of a chimpanzee mother toward her dead infant. Am J Primatol 73:415–421. https://doi.org/10.1002/ajp.20927
De Marco A, Cozzolino R, Thierry B (2018) Prolonged transport and cannibalism of mummified infant remains by a Tonkean macaque mother. Primates 59:55–59. https://doi.org/10.1007/s10329-017-0633-8
Dindo M, Thierry B, Whiten A (2008) Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc R Soc B 275:187–193. https://doi.org/10.1098/rspb.2007.1318
Engelbert LM (2018) The effects of the death of a group member on the behavior of tufted capuchins (Sapajus apella). Master Thesis, Franklin & Marshall College, Lancaster
Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL (2006) Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc R Soc B 273:707–712. https://doi.org/10.1098/rspb.2005.3378
Fashing PJ, Nguyen N, Barry TS, Goodale CB, Burke RJ, Jones SC, Kerby JT, Lee LM, Nurmi NO, Venkataraman VV (2010) Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology. Am J Primatol 73:405–409. https://doi.org/10.1002/ajp.20902
Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, Cambridge
Gonçalves A, Carvalho S (2019) Death among primates: a critical review of non-human primate interactions towards their dead and dying. Biol Rev 94:1502–1529. https://doi.org/10.1111/brv12512
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. https://doi.org/10.1007/s10329-012-0293-7
Perry S, Manson J (2008) Manipulative monkeys: the capuchins of Lomas Barbudal. Harvard University Press, Cambridge
Pruetz JD, Ontl KB, Cleaveland E, Lindshield S, Marshack J, Wessling EG (2017) Intragroup lethal aggression in West African chimpanzees (Pan troglodytes verus): inferred killing of a former alpha male at Fongoli, Senegal. Int J Primatol 38:31–57. https://doi.org/10.1007/s10764-016-9942-9949
Rajpurohit LS (1997) Why do mothers carry the corpses of their infants in Hanuman langurs, Presbytis entellus? J Nat Conserv 9:183–193
Speece MW, Brent SB (1984) Children’s understanding of death: a review of three components of a death concept. Child Dev 55:1671–1686. https://doi.org/10.2307/1129915
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. https://doi.org/10.1002/ajp.20994
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. https://doi.org/10.1537/ase.080919
Teleki G (1973) Group response to the accidental death of a chimpanzee in Gombe National Park, Tanzania. Folia Primatol 20:81–94. https://doi.org/10.1159/000155569
van Leeuwen EJC, Mulenga IC, Bodamer MD, Cronin KA (2016) Chimpanzees’ responses to the dead body of a 9-year-old group member. Am J Primatol 78:914–922. https://doi.org/10.1002/ajp.22560
Visalberghi E, Fragaszy D (1995) The behavior of capuchin monkeys, Cebus apella, with novel food: the role of social context. Anim Behav 49:1089–1095. https://doi.org/10.1006/anbe.1995.0137
Visalberghi E, Valente M, Fragaszy D (1998) Social context and consumption of unfamiliar foods by capuchin monkeys (Cebus apella) over repeated encounters. Am J Primatol 45:367–380. https://doi.org/10.1002/(SICI)1098-2345(1998)45:4%3c367:AID-AJP4%3e3.0.CO;2-U
Visalberghi E, Janson CH, Agostini I (2003) Response towards novel foods and novel objects in wild tufted capuchins (Cebus apella). Int J Primatol 24:653–675. https://doi.org/10.1023/A:1023700800113
Watson CFI, Matsuzawa T (2018) Behaviour of nonhuman primate mothers toward their dead infants: uncovering mechanisms. Phil Trans R Soc B 373:20170261. https://doi.org/10.1098/rstb.2017.0261
Yang B, Anderson JR, Li BG (2016) Tending a dying adult in a wild multi-level primate society. Curr Biol 26:R403–R404. https://doi.org/10.1016/j.cub.2016.03.062
Acknowledgements
We thank the managers and keepers of the Parco Faunistico di Piano dell’Abatino of Rieti for their technical support. We are grateful to Andrea Sanna, Pablo Rodriguez Ayuso, and Marta Canet Fernandez for their assistance.
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De Marco, A., Cozzolino, R. & Thierry, B. Responses to a dead companion in a captive group of tufted capuchins (Sapajus apella). Primates 61, 111–117 (2020). https://doi.org/10.1007/s10329-019-00743-y
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DOI: https://doi.org/10.1007/s10329-019-00743-y