Behaviour of nonhuman primate mothers toward their dead infants: uncovering mechanisms

Watson, Claire F I; Matsuzawa, Tetsuro

doi:10.1098/rstb.2017.0261

Cited by 63 publications

(128 citation statements)

References 39 publications

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“…In two of those cases, the infant died shortly after birth, the mother was still alive and the corpse was handled by a third individual, who provided greater post-mortem care than the mother. It has been argued that the lack of a strong bond if an infant dies soon after birth can result in decreased responsiveness of the mother to her infant [8]. However, our data contradict this interpretation of the social-bonds hypothesis: one mother showed extensive carrying of her neonate's corpse (Case 6), and two stillborn foetuses were also carried for several days, with both mothers appearing distressed at losing the corpse (Cases 1 and 5).…”

Section: Discussioncontrasting

confidence: 72%

“…What are the evolutionary origins of human mortuary practices and the awareness of mortality [4]?Most descriptions of animals' responses to death are anecdotal, and have focused on mothers' responses to the death of their infant ([3], for reviews of other cases, see [5][6][7]). This focus is circumstantial rather than a reflection of the putative importance of this particular behaviour for understanding responses to death: these cases are more frequently observed because of high infant mortality and the greater ability of mothers, particularly primates, to transport relatively small-bodied individuals after death [8]. Nonetheless, these records have been informative, with notable variation described in both individuals' and species' behaviour towards dead infants [9,10].…”

mentioning

confidence: 99%

“…These observations provide a good starting point for understanding the drivers of variation in individuals' responses towards dead infants. We briefly describe some of the main hypotheses for infant corpse carrying in primates below (for a more comprehensive list and review, see [8]). We focus on primates because these cases are the most commonly reported and have generated the greatest comparative thanatology literature thus far.The most commonly cited hypotheses to explain infant corpse carrying in bereaved primates, i.e.…”

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confidence: 99%

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Baboon thanatology: responses of filial and non-filial group members to infants' corpses

et al. 2020

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What do animals know of death? What can animals' responses to death tell us about the evolution of species’ minds, and the origins of humans' awareness of death and dying? A recent surge in interest in comparative thanatology may provide beginnings of answers to these questions. Here, we add to the comparative thanatology literature by reporting 12 cases of group members' responses to infants’ deaths, including 1 miscarriage and 2 stillbirths, recorded over 13 years in wild Namibian chacma baboons. Wild baboons' responses to dead infants were similar to other primates: in general, the mother of the infant carried the infants’ corpse for varying lengths of time (less than 1 h to 10 days) and tended to groom the corpses frequently, though, as in other studies, considerable individual differences were observed. However, we have not yet observed any corpse carriage of very long duration (i.e. greater than 20 days), which, though rare, occurs in other Old World monkeys and chimpanzees. We hypothesize this is due to the costs of carrying the corpse over the greater daily distances travelled by the Tsaobis baboons. Additionally, in contrast to other case reports, we observed male friends' ‘protection’ of the infant corpse on three occasions. We discuss the implications of these reports for current questions in the field.

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Section: Discussioncontrasting

confidence: 72%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Baboon thanatology: responses of filial and non-filial group members to infants' corpses

et al. 2020

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“…While some hypotheses have been proposed to explain post‐mortem carrying (Table ), it is still a matter of debate which one offers the most powerful explanation. Because some are mutually non‐exclusive it is likely that many factors, depending on context, contribute to these behaviours (see Watson & Matsuzawa, ).…”

Section: Primate Thanatology: Contemporary Reportsmentioning

confidence: 99%

“…Inexperienced Japanese macaque mothers have been observed to inadvertently drown their infants when diving into the hot springs of Jigokudani Park for food (de Waal, ) and similar occurrences have been reported among baboons (Cheney & Seyfarth, ). Moreover, filial cannibalism during post‐mortem carrying has also been witnessed, suggesting that corpses may be re‐categorised as food (Altmann, ; Hsiang‐Jen & Hsiu‐Hui, ; Dellatore, Waitt & Foitova, ; Watson et al , ; Tian et al , ; Tokuyama et al , ; De Marco, Cozzolino & Thierry, ; Watson & Matsuzawa, ).…”

Section: Primate Thanatology: Contemporary Reportsmentioning

confidence: 99%

Death among primates: a critical review of non‐human primate interactions towards their dead and dying

2019

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For the past two centuries, non-human primates have been reported to inspect, protect, retrieve, carry or drag the dead bodies of their conspecifics and, for nearly the same amount of time, sparse scientific attention has been paid to such behaviours. Given that there exists a considerable gap in the fossil and archaeological record concerning how early hominins might have interacted with their dead, extant primates may provide valuable insight into how and in which contexts thanatological behaviours would have occurred. First, we outline a comprehensive history of comparative thanatology in non-human primates, from the earliest accounts to the present, uncovering the interpretations of previous researchers and their contributions to the field of primate thanatology. Many of the typical behavioural patterns towards the dead seen in the past are consistent with those observed today. Second, we review recent evidence of thanatological responses and organise it into distinct terminologies: direct interactions (physical contact with the corpse) and secondary interactions (guarding the corpse, vigils and visitations). Third, we provide a critical evaluation regarding the form and function of the behavioural and emotional aspects of these responses towards infants and adults, also comparing them with non-conspecifics. We suggest that thanatological interactions: promote a faster re-categorisation from living to dead, decrease costly vigilant/caregiving behaviours, are crucial to the management of grieving responses, update position in the group's hierarchy, and accelerate the formation of new social bonds. Fourth, we propose an integrated model of Life-Death Awareness, whereupon neural circuitry dedicated towards detecting life, i.e. the agency system (animate agency, intentional agency, mentalistic agency) works with a corresponding system that interacts with it on a decision-making level (animate/inanimate distinction, living/dead discrimination, death awareness). Theoretically, both systems are governed by specific cognitive mechanisms (perceptual categories, associative concepts and high-order reasoning, respectively). Fifth, we present an evolutionary timeline from rudimentary thanatological responses likely occurring in earlier non-human primates during the Eocene to the more elaborate mortuary practices attributed to genus Homo throughout the Pleistocene. Finally, we discuss the importance of detailed reports on primate thanatology and propose several empirical avenues to shed further light on this topic. This review expands and builds upon previous attempts to evaluate the body of knowledge on this subject, providing an integrative perspective and bringing together different fields of research to detail the evolutionary, sensory/cognitive, developmental and historical/archaeological aspects of primate thanatology. Considering all these findings and given their cognitive abilities, we argue that non-human primates are capable of an implicit awareness of death.

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Mothers of disabled infants had higher cortisol levels in a free‐ranging group of Japanese macaques (Macaca fuscata)

Turner

Fedigan

Joyce

et al. 2023

American J Primatol

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Glucocorticoids (GCs) are hormones released in response to stressors and can provide insight into an organism's physiological well‐being. Experiencing chronic challenges to homeostasis is associated with significant deviations from baseline fecal GCs (fGCs) in many species, providing a noninvasive biomarker for assessing stress. In the group of free‐ranging Japanese macaques (Macaca fuscata) at the Awajishima Monkey Center in Japan, ~17% have congenital limb malformations. We collected 646 fecal samples from 27 females over three consecutive birth seasons (May–August) and analyzed them using enzyme immunoassay to extract fGCs. We explored the relationship between fGC levels and individual (physical impairment and reproductive status), social (dominance rank and availability of kin for social support), and ecological variables (exposure to potential predators, rainfall, and wild fruit availability). A disabled infant was associated significantly with higher fGC in the mother; however, physical impairment in adult females was not significantly related to fGC levels. Females with higher dominance rank had significantly lower fGC levels than lower ranking females. Other factors did not relate significantly to fGC. These results suggest that providing care that meets the support needs of disabled infants poses a physiological challenge for mothers and suggests that physically impaired adults are able to effectively compensate for their disabilities with behavioral plasticity. Once an individual with congenital limb malformations survives infancy through their mother's care, physical impairment does not appear to influence fGC values, while social variables like dominance rank significantly influenced cortisol values in free‐ranging female Japanese macaques.

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Behaviour of nonhuman primate mothers toward their dead infants: uncovering mechanisms

Cited by 63 publications

References 39 publications

Baboon thanatology: responses of filial and non-filial group members to infants' corpses

Baboon thanatology: responses of filial and non-filial group members to infants' corpses

Death among primates: a critical review of non‐human primate interactions towards their dead and dying

Mothers of disabled infants had higher cortisol levels in a free‐ranging group of Japanese macaques (Macaca fuscata)

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