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Thanatology in the northern muriqui (Brachyteles hypoxanthus)

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Abstract

Primate thanatology, or the study of primate responses to dying and death, has become increasingly relevant in recent years. However, the number of reports remains small and the quality of published records is highly variable. Here, we extend the literature on comparative thanatology with observations on a population of the northern muriqui (Brachyteles hypoxanthus). We compiled all seven cases of muriqui responses to dead, dying, or abandoned infants observed by trained researchers of the Muriqui Project of Caratinga between 1998 and 2020. Four different adult females were observed carrying their dead offspring (n = 4) and one of these females was also observed carrying her dead grand-offspring (n = 1). Five of the seven cases involved dead newborns, one involved a newborn abandoned by its mother on the forest floor, and one involved a 1.6-year-old infant that was visibly ill and died after its mother left it on the ground. Dead newborns were carried for 1–3 days, and all cases occurred during the dry season months. No other age-sex classes were observed to interact with the dead or dying immatures. Our observations are consistent with hypotheses concerning the predominance of dead-infant carrying in other primates, and with the effects of climate on rates of corpse disintegration. They also show the value of long-term studies for obtaining and understanding anecdotal records of rare behavior.

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  • 11 June 2022

    The article has been updated to add the ORCID ID of co-corresponding author.

References

  • Alley TR (1980) Infantile colouration as an elicitor of caretaking behaviour in Old World primates. Primates 21:416–429

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Anderson JR (2017) Comparative evolutionary thanatology of grief, with special reference to nonhuman primates. JRCA 18:173–189

    Google Scholar 

  • Anderson JR (2020) Responses to death and dying: primates and other mammals. Primates 61:1–7

    Article  PubMed  Google Scholar 

  • Anderson JR, Gillies A, Lock LC (2010) Pan thanatology. Curr Biol 20:349–351

    Article  CAS  Google Scholar 

  • Andrade BM, Freire-Filho R, Bezerra B (2020) The behaviours of a female blonde capuchin (Sapajus flavius) towards her dead infant. Behaviour 157:1231–1238

    Article  Google Scholar 

  • Assunção ML, Mendes SL, Strier KB (2007) Grandmaternal infant carrying in wild northern muriquis (Brachyteles hypoxanthus). Neotrop Primates 14:120–122

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Boubli JP, Couto-Santos F, Strier KB (2011) Structure and floristic composition of one of the last forest fragments containing the critically endangered northern muriqui (Brachyteles hypoxanthus, Primates). Ecotropica 17:53–69

    Google Scholar 

  • Bronikowski AM, Cords M, Alberts SC, Altmann J, Brockman DK, Fedigan LM, Pusey A, Stoinski T, Strier KB, Morris WF (2016) Female and male life tables for seven wild primate species. Sci Data 3:1–8

    Article  Google Scholar 

  • Buhl JS, Aure B, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML, Brent LJ (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 

  • Campbell LA, 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

    Article  PubMed  Google Scholar 

  • Carter AJ, Baniel A, Cowlishaw G, Huchard E (2020) Baboon thanatology: responses of filial and non-filial group members to infants’ corpses. R Soc Open Sci 7:1–17

    Article  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Fashing PJ, Nguyen N, Barry TS, Goodalle CB, Burke RJ, Jones SCZ, Kerby JT, Lee LM, Nurmi NO, Venkata 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 

  • Goldenberg SZ, Wittemyer G (2020) Elephant behavior toward the dead: a review and insights from field observations. Primates 61:119–128

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Guedes D, Young RJ, Strier KB (2008) Energetic costs of reproduction in female northern muriquis, Brachyteles hypoxanthus (Primates: Platyrrinhi: Atelidae). Rev Bras Zool 25:587–593

    Article  Google Scholar 

  • Guimarães VO, Strier KB (2001) Adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus). Primates 42:395–399

    Article  Google Scholar 

  • Jay PC (1962) Aspects of maternal behavior among langurs. Ann N Y Acad Sci 102:468–476

    Article  CAS  PubMed  Google Scholar 

  • Kaizer MC, Coli AZ, Mendes SL, Strier KB (2011) Interações de machos adultos e infantes em Brachyteles hypoxanthus (Kuhl 1820). In: Miranda JMD, Hirano ZMB (eds) A Primatologia no Brasil 12. UFPR/Sociedade Brasileira de Primatology Curitiba, Pára, pp 2016–2220

    Google Scholar 

  • 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 

  • Lonsdorf EV, Wilson ML, Boehm E, Delaney-Soesman J, Grebey T, Murray C, Pusey AE (2020) Why chimpanzees carry dead infants: an empirical assessment of existing hypotheses. R Soc Open Sci 7:1–15

    Article  Google Scholar 

  • Martins WP, Guimarães VO, Strier KB (2007) A case of infant swapping by wild northern muriquis (Brachyteles hypoxanthus). Primates 48:324–326

    Article  PubMed  Google Scholar 

  • Matsuzawa T (1997) The death of an infant chimpanzee at Bossou, Guinea. Pan Afr News 4:4–6

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nakagawa N (2021) Observation and publication of infrequently observed behavior. Primates 62:549–554

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicolson NA (1991) Maternal behavior in human and nonhuman primates. In: Loy JD, Peters CB (eds) Understanding behavior: what primate studies tell us about human behavior. Oxford University Press, Oxford, pp 17–50

    Google Scholar 

  • Ramsay MS, Teichroeb JA (2019) Anecdotes in primatology: temporal trends, anthropocentrism, and hierarchies of knowledge. Am Anthropol 121:680–693

    Article  Google Scholar 

  • Sharma G, Bharti S, Chena R, Rajpurohit LS (2011) Dead infant carrying in the Hanuman langur (Semnopithecus entellus) around Jodhpur (Rajasthan). Lab Prim Newslett 50:1–5

    Google Scholar 

  • Sharma N, Pokharel SS, Kohshima S, Sukumar R (2020) Behavioural responses of free-ranging Asian elephants (Elephas maximus) towards dying and dead conspecifics. Primates 61:129–138

    Article  PubMed  Google Scholar 

  • 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 

  • Strier KB (1990) New World primates, new frontiers: insights from the woolly spider monkey, or muriqui (Brachyteles arachnoides). Int J Primatol 11:7–19

    Article  Google Scholar 

  • Strier KB (1996) Reproductive ecology of female muriquis. In: Norconk M, Rosenberger A, Garber P (eds) Adaptive radiations of Neotropical primates. Plenum Press, New York, pp 511–532

    Chapter  Google Scholar 

  • Strier KB (2019) Everything for the muriquis: reflections from a long-term field study of a critically endangered primate. Boletim Soc Bras Mastozool. 85:117–127

    Google Scholar 

  • Strier KB (2021) Editorial: the limits of resilience. Primates 62:861–868

    Article  PubMed  Google Scholar 

  • Strier KB, Altmann J, Brockman DK, Bronikowski AM, Cords M, Fedigan LM, Alberts SC (2010) The primate life history database: a unique shared ecological data resource. Methods Ecol Evol 1:199–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Strier KB, Boubli JP (2006) A history of long-term research and conservation of northern muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA. Primat Conserv 2006:53–63

    Article  Google Scholar 

  • Strier KB, Mendes SL (2012) The northern muriqui (Brachyteles hypoxanthus): lessons on behavioral plasticity and population dynamics from a critically endangered species. In: Kappeler P, Watts D (eds) Long-term field studies of primates. Springer, Heidelberg, pp 125–140

    Chapter  Google Scholar 

  • Strier KB, Mendes SL, Santos RR (2001) Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus). Am J Primatol 55:87–100

    Article  CAS  PubMed  Google Scholar 

  • Strier KB, Dib LT, Figueira JEC (2002) Social dynamics of male muriquis (Brachyteles arachnoides hypoxanthus). Behaviour 138:315–342

    Google Scholar 

  • Strier KB, Chaves PB, Mendes SL, Fagundes V, Di Fiore A (2011) Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. Proc Natl Acad Sci U S A 108:18915–18919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strier KB, Possamai CB, Mendes SL (2015) Dispersal patterns of female northern muriquis: implications for social dynamics, life history, and conservation. In: Furuichi T, Yamagiwa J, Aureli F (eds) Dispersing primate femalea. Springer, Tokyo, pp 3–22

    Chapter  Google Scholar 

  • 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 

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

    Article  CAS  Google Scholar 

  • Thompson CL, Hrit R, Melo LC, Vinyard CJ, Bottenberg KN, de Oliveira MA (2020) Callitrichid responses to dead and dying infants: the effects of paternal bonding and cause of death. Primates 61:707–716

    Article  PubMed  Google Scholar 

  • Tolentino K, Roper JJ, Passos FC, Strier KB (2008) Mother–offspring associations in northern muriquis, Brachyteles hypoxanthus. Am J Primatol 70:301–305

    Article  PubMed  Google Scholar 

  • van Leeuwen EJ, 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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Watson CF, Matsuzawa T (2018) Behaviour of nonhuman primate mothers toward their dead infants: uncovering mechanisms. Philos Trans R Soc Lond B Biol Sci 373:1–11

    Google Scholar 

  • Watts DP (2020) Responses to dead and dying conspecifics and heterospecifics by wild mountain gorillas (Gorilla beringei beringei) and chimpanzees (Pan troglodytes schweinfurthii). Primates 61:55–68

    Article  PubMed  Google Scholar 

  • Wroblewski EE (2008) An unusual incident of adoption in a wild chimpanzee (Pan troglodytes) population at Gombe National Park. Am J Primatol 70(10):995–998

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) of the Brazilian government, and Ramiro Abdalla of Preserve Muriqui for permission to conduct this research at the RPPN Feliciano Miguel Abdala. We thank all of the people and funding agencies that have supported this fieldwork over the years, as listed in: https://strierlab.anthropology.wisc.edu/muriqui-project-of-caratinga-acknowledgements/. We especially thank the staff of the reserve, including Vera, Roberto, Jairo, Antonio Bragança and everyone who lives in the community; Conservation International and Preserve Muriqui for administrative and logistical support to the project; and all of the researchers from Projeto Muriqui de Caratinga who responded to our initial email inquiry for descriptions of muriqui behavior toward dead or dying conspecifics: Samara Luiza, Renan Cézar, Valéria Cristina, Jefferson Cordeiro, Jeronimo Sanguinetti, Anamélia de Souza Jesus, Thiago Cavalcante, Fabricio Fernandes, Ana Biatriz Siqueira, Mariane Kaizer, Vagner de Souza, and Luiz G. Dias. We also wish to thank the editor and reviewers for their helpful and insightful comments, which greatly improved this manuscript.

Funding

Support for fieldwork component of this long-term project was to KBS from the following sources: National Science Foundation, BNS 8305322, BCS 8619442, BCS 8958298, BCS 9414129, BCS 0621788, BCS 0921013; National Geographic Society; Liz Claiborne Art Ortenberg Foundation; Fulbright Foundation; Sigma Xi Grants-in-Aid; Henry M. Jackson Foundation, grant no. 213; World Wildlife Fund; The Leakey Foundation; Chicago Zoological Society; Lincoln Park Zoo Neotropic Fund; Center for Research on Endangered Species; Margot Marsh Biodiversity Foundation; Conservation International; Primate Action Fund; Muriqui Instituto de Biodiversidade; Graduate School of the University of Wisconsin-Madison; University of Wisconsin-Madison; a Hilldale Professorship; a Vilas Research Professorship; Microsoft Corporation Employee Salesforce Matching Gifts Program; and Re:Wild (previously Global Wildlife Conservation). Support during the preparation of this manuscript to RFF was from Rufford Foundation (Grant Number: 196461) and FACEPE (Fundação de Amparo à Ciência e Tecnologia de Pernambuco, # IBPG-1236-2.05/16).

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Correspondence to Robério Freire Filho or Karen B. Strier.

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The article has been updated to add the ORCID ID of co-corresponding author.

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Freire Filho, R., Inforzato, I., Tabacow, F.P. et al. Thanatology in the northern muriqui (Brachyteles hypoxanthus). Primates 63, 335–342 (2022). https://doi.org/10.1007/s10329-022-00991-5

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