Reaction to allospecific death and to an unanimated gorilla infant in wild western gorillas: insights into death recognition and prolonged maternal carrying

Abstract

It is still unclear to what extent animals possess knowledge of death. Primates display a large variety and often contradictory behaviors toward conspecific corpses, particularly those of infants (e.g., prolonged carrying and care). This study reports on reactions in a wild, habituated western gorilla group (Gorilla gorilla, 11–13 individuals) in the Central African Republic to an unanimated conspecific infant, and to an allospecific corpse. Individuals’ reactions were compared to their usual behavior using both continuous focal animal sampling and 10-min instantaneous scan sampling. In the first observation, an infant gorilla fell out of a tree and looked dead. The mother retrieved it and remained unusually close to another adult female, until the infant started to move again, almost 1 h later. Cases of infants regaining consciousness after almost-fatal accidents may act as positive reinforcement for continued carrying by mothers, which might be socially learned. In the second case, three immature gorillas reacted to a dead red river hog. For 20 min they stared at the corpse from tree branches above, while chest beating, defecating, and urinating several times. They showed fear and did not approach the corpse. These observations show that non-predatory species, such as gorillas, may be able to acquire and develop some knowledge about death even though they do not kill other vertebrates.

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References

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

    CAS  Google Scholar 

  2. Anderson JR (2011) A primatological perspective on death. Am J Primatol 73:410–414. https://doi.org/10.1002/ajp.20922

    Article  PubMed  PubMed Central  Google Scholar 

  3. Anderson JR (2019) Responses to death. In: Choe JC (ed) Encyclopedia of animal behavior, vol 1, 2nd edn. Elsevier, Amsterdam, pp 424–428

    Google Scholar 

  4. Anderson JR, Gillies A, Lock LC (2010) Pan thanatology. Curr Biol 20:R349–R351. https://doi.org/10.1016/j.cub.2010.02.010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Anderson JR, Gillies A, Lock LC (2016) Comparative thanatology. Curr Biol 26:R553–R556

    CAS  Article  Google Scholar 

  6. Anderson JR, Biro D, Pettitt P (2018) Evolutionary thanatology. Phil Trans R Soc B 373:20170262. https://doi.org/10.1098/rstb.2017.0262

    Article  PubMed  Google Scholar 

  7. Appleby R, Smith B, Jones D (2013) Observations of a free-ranging adult female dingo (Canis dingo) and littermates’ responses to the death of a pup. Behav Process 96:42–46. https://doi.org/10.1016/j.beproc.2013.02.016

    Article  Google Scholar 

  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300 (MR 1325392)

    Google Scholar 

  9. Biro D (2011) Chimpanzee mothers carry the mummified remains of their dead infants: three case reports from Bossou. In: Matsuzawa T, Humle T, Sugiyama Y (eds) The chimpanzees of Bossou and Nimba. Springer, Tokyo, pp 241–250

    Google Scholar 

  10. 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. https://doi.org/10.1016/j.cub.2010.02.031

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Boesch C (1991) Teaching among wild chimpanzees. Anim Behav 41:530–532

    Article  Google Scholar 

  12. Boesch C (2012) Wild cultures: a comparison between chimpanzee and human cultures. Cambridge University Press, Cambridge

    Google Scholar 

  13. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the Taï National Park. Am J Phys Anthropol 78:547–573. https://doi.org/10.1002/ajpa.1330780410

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taï Forest: behavioural ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  15. Bonoti F, Leonardi A, Mastora A (2013) Exploring children’s understanding of death: through drawings and the death concept questionnaire. Death Stud 37:47–60. https://doi.org/10.1080/07481187.2011.623216

    Article  PubMed  Google Scholar 

  16. Breuer T, Hockemba MBN, Olejniczak C, Parnell RJ, Stokes EJ (2008) Physical maturation, life-history classes and age estimates of free-ranging western gorillas insights from Mbeli Bai, Republic of Congo. Am J Primatol 71:106–119

    Article  Google Scholar 

  17. 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

    Article  PubMed  PubMed Central  Google Scholar 

  18. Carvalho S, Yamanashi Y, Yamakoshi G, Matsuzawa T (2010) Bird in the hand: Bossou chimpanzees (Pan troglodytes) capture West African wood-owls (Ciccaba woodfordi) but not to eat. Pan Afr News 17:6–9

    Article  Google Scholar 

  19. Cibot M, Sabiiti T, McLennan MT (2017) Two cases of chimpanzees interacting with dead animals without food consumption at Bulindi, Hoima District, Uganda. Pan Afr News 24(1):6–8

    Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. Devaine M, San-Galli A, Trapanese C, Bardino G, Hano C, Saint Jalme M et al (2017) Reading wild minds: a computational assay of Theory of Mind sophistication across seven primate species. PLoS Comput Biol 13(11):e1005833. https://doi.org/10.1371/journal.pcbi.1005833

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Doran DM, McNeilage A, Greer D, Bocian C, Mehlman P, Shah N (2002) Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on indirect sampling methods. Am J Primatol 58:91–116

    Article  Google Scholar 

  23. Doran-Sheehy D, Shah N, Heimbauer L (2006) Sympatric western gorilla and mangabey diet: re-examination of ape and monkey foraging strategies. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates: ecological, physical and behavioral aspects. Cambridge University Press, New York, pp 49–72

    Google Scholar 

  24. 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. https://doi.org/10.1016/j.applanim.2006.04.014

    Article  Google Scholar 

  25. 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. https://doi.org/10.1002/ajp.20902

    Article  PubMed  Google Scholar 

  26. Gonçalves A, Biro D (2018) Comparative thanatology, an integrative approach: exploring sensory/cognitive aspects of death recognition in vertebrates and invertebrates. Phil Trans R Soc B 373:20170263. https://doi.org/10.1098/rstb.2017.0263

    Article  PubMed  Google Scholar 

  27. Gonçalves A, Carvalho S (2019) Death among primates: a critical review of non-human primate interactions towards their dead and dying. Biol Rev. https://doi.org/10.1111/brv.12512

    Article  PubMed  Google Scholar 

  28. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  29. Harcourt AH (1979) Social relationships among adult female mountain gorillas. Anim Behav 27:251–264. https://doi.org/10.1016/0003-3472(79),90145-3

    Article  Google Scholar 

  30. Harcourt AH, Stewart KJ (2007) Gorilla society. Conflict, compromise and cooperation between sexes. University of Chicago Press, Chicago

    Google Scholar 

  31. Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61:139–151. https://doi.org/10.1006/anbe.2000.1518(PMID: 11170704)

    Article  PubMed  Google Scholar 

  32. Harzen S, dos Santos ME (1992) Three encounters with wild bottlenose dolphins (Tursiops truncates) carrying dead calves. Aquat Mamm 18:49–55

    Google Scholar 

  33. Haskins CP, Haskins EF (1974) Notes on necrophoric behavior in the archaic ant Myrmecia vindex (Formicidae: Myrmeciinae). Psyche 81:258–267. https://doi.org/10.1155/1974/80395

    Article  Google Scholar 

  34. Hedwig D, Hammerschmidt K, Mundry R, Robbins MM, Boesch C (2014) Acoustic structure and variation in mountain and western gorilla close calls: a syntactic approach. Behaviour 151:1091–1120

    Article  Google Scholar 

  35. Hirata S, Yamakoshi G, Fujita S, Ohashi G, Matsuzawa T (2001) Capturing and toying with hyraxes (Dendrohyrax dorsalis) by wild chimpanzees (Pan troglodytes) at Bossou, Guinea. Am J Primatol 53:93–97. https://doi.org/10.1002/1098-2345(200102)53:2,93:aid-ajp5.3.0.co;2-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Hockings KJ, Humle T, Carvalho S, Matsuzawa T (2012) Chimpanzee interactions with nonhuman species in an anthropogenic habitat. Behaviour 149:299–324. https://doi.org/10.1163/156853912X636735

    Article  Google Scholar 

  37. Hoff MP, Hoff KT, Maple TL (1998) Behavioural response of a western lowland gorilla (Gorilla gorilla gorilla) group to the loss of the silverback male at Zoo Atlanta. Int Zoo Ybk 36:90–96

    Article  Google Scholar 

  38. Hrdy SB (1999) Mother nature: maternal instincts and how they shape the human species. Ballantine Books, New York

    Google Scholar 

  39. Humle T, Snowdon CT, Matsuzawa T (2009) Social influences on ant-dipping acquisition in the wild chimpanzees (Pan troglodytes verus) of Bossou, Guinea, West Africa. Anim Cogn 12:S37–S48

    Article  Google Scholar 

  40. Hussain A, Saraiva LR, Ferrero DM, Ahuja G, Krishna VS, Liberles SD, Korsching SI (2013) High-affinity olfactory receptor for the death-associated odor cadaverine. Proc Natl Acad Sci USA 110(579–19):584. https://doi.org/10.1073/pnas.1318596110

    CAS  Article  Google Scholar 

  41. Kano T (1992) The last ape: pygmy chimpanzee behaviour and ecology. Stanford University Press, Stanford

    Google Scholar 

  42. 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. Primates 53:127–132

    Article  Google Scholar 

  43. Lonsdorf EV (2006) What is the role of mothers in the acquisition of termite-fishing behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? Anim Cogn 9:36–46

    Article  Google Scholar 

  44. Masi S, Bouret S (2015) Odor signals in wild western lowland gorillas: an involuntary and extra-group communication hypothesis. Physiol Behav 145:123–126

    CAS  Article  Google Scholar 

  45. Masi S, Breuer T (2018) Dialium seed coprophagy in wild western gorillas: multiple nutritional benefits and toxicity reduction hypotheses. Am J Primatol. https://doi.org/10.1002/ajp.22752

    Article  PubMed  Google Scholar 

  46. Masi S, Cipolletta C, Robbins MM (2009) Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory. Am J Primatol 71:91–100

    Article  Google Scholar 

  47. Masi S, Gustaffson E, Saint Jalme M, Narat V, Todd A, Bomsel MC, Krief S (2012) Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: role of sociality and physiology on learning process. Physiol Behav 105:337–349

    CAS  Article  Google Scholar 

  48. Masi S, Mundry R, Ortmann S, Cipolletta C, Boitani L, Robbins MM (2015) The influence of seasonal frugivory on nutrient and energy intake in wild western gorillas. PLoS One 10:e0129254

    Article  Google Scholar 

  49. McLennan MR (2010) Chimpanzee ecology and interactions with people in an unprotected human-dominated landscape at Bulindi, Western Uganda. PhD dissertation. Oxford Brookes University, UK

  50. Moss C (1988) Elephant memories: thirteen years in the life of an elephant family. William Morrow and Co, New York

    Google Scholar 

  51. Oliveira TA, Koakoski G, da Motta AC, Piato AL, Barreto RE, Volpato GL, Barcellos LJG (2014) Death-associated odors induce stress in zebrafish. Horm Behav 65:340–344. https://doi.org/10.1016/j.yhbeh.2014.02.009

    Article  PubMed  Google Scholar 

  52. Peterson RS, Batholomew GA (1967) The natural history and behavior of the California sea lion. Am Soc Mamm 737:47–98

    Google Scholar 

  53. Pohlert T (2016) The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). R package. http://CRAN.R-project.org/package=PMCMR

  54. Porter A, Eckardt W, Vecellio V, Guschanski K, Niehoff PP, Ngobobo-As-Ibungu U, Nishuli Pekeyake R, Stoinski T, Caillaud D (2019) Behavioral responses around conspecific corpses in adult eastern gorillas (Gorilla beringei spp.). PeerJ 7:e6655. https://doi.org/10.7717/peerj.6655

    Article  PubMed  PubMed Central  Google Scholar 

  55. Prounis GS, Shields WM (2013) Necrophobic behavior in small mammals. Behav Process 94:41–44. https://doi.org/10.1016/j.beproc.2012.12.001

    Article  Google Scholar 

  56. Reggente MAL, Alves F, Nicolau C, Freitas L, Cagnazzi D, Baird RW, Galli P (2016) Nurturant behavior toward dead conspecifics in free-ranging mammals: new records for odontocetes and a general review. J Mamm 97:1428–1434. https://doi.org/10.1093/jmammal/gyw089

    Article  Google Scholar 

  57. Reggente MALV, Papale E, McGinty N, Eddy L, de Lucia GA, Bertulli CG (2018) Social relationships and death-related behaviour in aquatic mammals: a systematic review. Phil Trans R Soc B 373:20170260. https://doi.org/10.1098/rstb.2017.0260

    Article  PubMed  Google Scholar 

  58. Remis MJ (1997) Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am J Primatol 43:87–109

    CAS  Article  Google Scholar 

  59. Sabater Pi J, Bermejo M, Illera G, Vea JJ (1993) Behavior of bonobos (Pan paniscus) following their capture of monkeys in Zaire. Int J Primatol 14:797–804. https://doi.org/10.1007/BF02192191

    Article  Google Scholar 

  60. Salmi R, Hammerschmidt K, Doran-Sheehy DM (2014) Individual distinctiveness in call types of wild western female gorillas. PLoS One 9(7):e101940

    Article  Google Scholar 

  61. Schmelz M, Call J, Tomasello M (2011) Chimpanzees know that others make inferences. Proc Natl Acad Sci 108:3077–3079. https://doi.org/10.1073/pnas.1000469108(PMID: 21282649)

    Article  PubMed  Google Scholar 

  62. Sharma G, Swami B, Ram C, Rajpurohit LS (2010) Dead infant carrying in the Hanuman Langur (Semnopithecus entellus) around Jodhpur (Rajasthan). Lab Prim Newsl 50:1–5

    Google Scholar 

  63. 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

    Article  PubMed  PubMed Central  Google Scholar 

  64. 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

    Article  Google Scholar 

  65. Teleki G (1973) Group response to the accidental death of a chimpanzee in Gombe National Park, Tanzania. Folia Primatol 20:81–94

    CAS  Article  Google Scholar 

  66. Tian J, Zhang S, Guo Y, Garber PA, Guo W, Kuang S, Lu J (2016) Evidence of placentophagia and mother–infant cannibalism in free-ranging Macaca mulatta tcheliensis in Mount Taihangshan, Jiyuan, China. Folia Primatol 87:381–391. https://doi.org/10.1159/000455845

    Article  PubMed  Google Scholar 

  67. Tokuyama N, Moore DL, Graham KE, Lokasola A, Furuichi T (2017) Cases of maternal cannibalism in wild bonobos (Pan paniscus) from two different field sites, Wamba and Kokolopori, Democratic Republic of the Congo. Primates 58:7–12. https://doi.org/10.1007/s10329-016-0582-7

    Article  PubMed  Google Scholar 

  68. Trapanese C, Bey M, Tonachella G, Meunier H, Masi S (2019) Infant cannibalism from relatives in semi-free ranging capuchins. Primates (this issue)

  69. van de Rijt-Plooij HHC, Plooij FX (1987) Growing independence, conflict and learning in mother–infant relations in free-ranging chimpanzees. Behaviour 101:1–86. https://doi.org/10.1163/156853987X00378

    Article  Google Scholar 

  70. Veit PG (1982) Gorilla society. Nat Hist 91:48–59

    Google Scholar 

  71. Warren Y, Williamson EA (2004) Transport of dead infant mountain gorillas by mothers and unrelated females. Zoo Biol 23:375–378. https://doi.org/10.1002/zoo.20001

    Article  Google Scholar 

  72. Watson CFI, Matsuzawa T (2018) Behaviour of nonhuman primate mothers toward their dead infants: uncovering mechanisms. Phil Trans R Soc 373:20170261. https://doi.org/10.1098/rstb.2017.0261

    Article  Google Scholar 

  73. Watson CFI, Hashimoto N, Takayoshi N, Okamoto M, Matsuzawa T (2015) Two cases of dead-infant carrying followed by mother-infant cannibalism in captive socially housed Japanese macaques. Folia Primatol 86:378–379

    Google Scholar 

  74. Williamson EA (2014) Mountain gorillas: a shifting demographic landscape. In: Yamagiwa J, Karczmarski L (eds) Primates and cetaceans: field research and conservation of complex mammalian societies. Springer, Tokyo, pp 273–287

    Google Scholar 

  75. Wilson EO, Durlach NI, Roth LM (1958) Chemical releaser of necrophoric behavior in ants. Psyche 65:108–114. https://doi.org/10.1155/1958/69391

    Article  Google Scholar 

  76. Wisman A, Shrira I (2015) The smell of death: evidence that putrescine elicits threat management mechanisms. Front Psychol 6:1274. https://doi.org/10.3389/fpsyg.2015.01274

    Article  PubMed  PubMed Central  Google Scholar 

  77. Yamamoto S, Humle T, Tanaka M (2012) Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals. Proc Natl Acad Sci 109:3588–3592. https://doi.org/10.1073/pnas.1108517109(PMID: 22315399)

    Article  PubMed  Google Scholar 

  78. Zamma K (2002) A chimpanzee trifling with a squirrel: pleasure derived from teasing? Pan Afr News 9:9–11

    Article  Google Scholar 

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Acknowledgements

I thank Dr. James Anderson for the invitation to contribute to this special issue and for the careful editing of the manuscript. I thank the Ministers of Education and Water and Forests, Fishing and Hunting of the Central African Republic (CAR) government for permission to conduct this research. I am grateful to Angelique Todd of WWF CAR, at that time managing the Primate Habituation Program of Dzanga-Sangha Protected Areas (DSPA) and to the Administration of DSPA, and the Bai-Hokou staff in CAR for facilitating logistics and permissions. I thank Damien Caillaud and an anonymous reviewer for very useful comments on the manuscript. I thank the Muséum national d’Histoire naturelle, ATM (Action Transversale du Muséum), and Sabrina Krief and the ANR JC SAFAPE for their institutional and financial support. Special thanks go to the Aka trackers for their courageous and essential work.

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Masi, S. Reaction to allospecific death and to an unanimated gorilla infant in wild western gorillas: insights into death recognition and prolonged maternal carrying. Primates 61, 83–92 (2020). https://doi.org/10.1007/s10329-019-00745-w

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Keywords

  • Thanatology
  • Prolong maternal carrying
  • Death consciousness
  • Reaction to dead allospecifics
  • Western gorillas