Comparative Evolutionary Thanatology of Grief, with Special Reference to Nonhuman Primates

James R. Anderson Kyoto University

Abstract: The impact of the dead on the living is considered from an evolutionary comparative perspective. After a brief review of young children’s developing understanding of the concept of death, the interest of looking at how other species respond to dying and dead individuals is introduced. Solutions to managing dead individuals in social insect communities are described, highlighting evolutionarily ancient, effective behavioral mechanisms that most likely function with no emotional component. I then review examples of responses to dying and dead individuals in nonhuman primates, with particular reference to continued transport and caretaking of dead infants, responses to traumatic deaths in wild populations of monkeys and apes, and a detailed case report of the peaceful death of an old female chimpanzee surrounded by members of her group. The emotional correlates of primates’ reactions to bereavement are discussed, and some suggested evolutionarily shared responses to the dead are proposed.

Key words: thanatology, death, dying, emotions, social insects, nonhuman primates, chimpanzees

Thanatology can be broadly defined as the study of death and dying, and researchers from a wide range of disciplines are thanatologists. Among others, studies in medicine, biology, psychology, anthropology, palaeontology, sociology and philosophy all contribute new knowledge about the antecedents, causes, and consequences of death (e.g. Exley 2004; Haldane 2007; Klarsfeld et al. 2003; Kübler-Ross 1969; Pettitt 2011; Powner et al. 1996). Concerning people’s understanding of death, psychologists generally agree that the typical human adult’s concept of death comprises at least four sub-concepts or “components” (Speece 1995). “Irreversibility” refers to the understanding that dead organisms cannot recover or be brought back to life. “Inevitability” (or universality) refers to the understanding that all living things eventually die, including oneself. “Non-functionality” (sometimes referred to as finality) refers to the understanding that a dead organism cannot behave, feel, perceive, think, or process information. “Causality” refers to understanding what underlies death, i.e., that it results from serious damage to or the breakdown of one or more vital bodily organs.

Japanese Review of Cultural Anthropology, vol. 18-1, 2017 174 James R. Anderson

In their investigations of how an adult-like concept of death is formed, developmental psychologists have shown that young children’s and adults’ views differ in several ways (for overviews see Slaughter 2005; Speece 1995). The differences concern the four recognized components of death understanding: universality (or inevitability), irreversibility, non-functionality, and causality. For example, instead of understanding the inevitability of death, young children typically believe that they and/or significant others in their lives will not die. Contra irreversibility, young children may also believe it is possible to come alive again after dying; being dead is akin to being asleep. Also for young children, a dead individual may still be sentient, able to perceive sensory stimulation such as people talking to them or touching them. Finally, children’s understanding that death is caused by damage to vital organs is preceded by a phase of prioritizing external causes, such as accidents, or killing. As will be seen later, these four components of death understanding can provide a useful perspective from which to look at the issue in other species, in particular other primates. Children typically achieve a mature understanding of death by the age of 10-11 years, when they are approaching Piaget’s stage of “formal operations” and show increased competence at dealing with abstract concepts (Inhelder and Piaget 1958). A grasp of the biological causes of death is the last component to be acquired, with the others being understood a few years earlier (Slaughter and Griffiths 2007; Speece and Brent 1984). Some evidence suggests that children with personal experience of bereavement – resulting from the demise of a family member, for example – have a more mature appreciation of irreversibility and non-functionality, along with an enhanced overall understanding of death. Depictions of death in drawings may also differ as a function of bereavement experience in childhood (Bonoti et al. 2013). Alongside academic and applied interest in how modern humans deal with death and dying, some thanatologists embrace evolutionary approaches. For example, palaeontologists and physical anthropologists attempt to piece together the emergence and development of corpse disposal practices among prehistoric and later hominids (e.g., Pettitt 2011). Biologists and ethologists study other species’ responses to dead and dying individuals from the perspectives of natural selection and underlying biological and psychological mechanisms (Anderson 2016; Archer 1999; King 2016). In the remainder of this article I review some thanatological research on nonhuman animals, with a particular focus on behavioral and emotional responses to corpses in nonhuman primates. I then propose a tentative comparison of some responses to the dead observed in modern humans and in our nearest evolutionary neighbors, chimpanzees. My overall aim is to elucidate some commonalities between how humans and nonhumans deal with their dead, and to argue that increased knowledge of the impact of the dead on living nonhumans can help our understanding of the evolution of modern humans’ concepts of and reactions to death.

James R. Anderson Grief in Nonhuman Animals 175

In their investigations of how an adult-like concept of death is formed, developmental Managing the Dead is Evolutionarily Ancient: Social Insects psychologists have shown that young children’s and adults’ views differ in several ways (for overviews see Slaughter 2005; Speece 1995). The differences concern the four Decaying corpses are a potential source of disease, especially if the deaths have arisen recognized components of death understanding: universality (or inevitability), irreversibility, from infection. The living may have better survival prospects if they avoid contact with non-functionality, and causality. For example, instead of understanding the corpses. Such avoidance is relatively easy to achieve for species or groups that have no inevitability of death, young children typically believe that they and/or significant particular fixed “home base” within their home range or territory. In primates, for others in their lives will not die. Contra irreversibility, young children may also believe it example, if a group member dies at or near one of the group’s sleeping sites, the corpse is possible to come alive again after dying; being dead is akin to being asleep. Also for can be avoided simply by moving away to another part of the home range and sleeping young children, a dead individual may still be sentient, able to perceive sensory at another location until risks associated with the proximity of the corpse have stimulation such as people talking to them or touching them. Finally, children’s diminished. Indeed, monkeys and apes typically leave dead individuals – with the understanding that death is caused by damage to vital organs is preceded by a phase of exception of dead infants (see below) – either precisely at or near to where they died, prioritizing external causes, such as accidents, or killing. As will be seen later, these after periods of time ranging from a few minutes to several hours (see below). Modern four components of death understanding can provide a useful perspective from which to hunter-gatherers have also been recorded to abandon camp following the death of group look at the issue in other species, in particular other primates. members (e.g., Lee, 1979). In nonhuman primates, by the time the surviving group- Children typically achieve a mature understanding of death by the age of 10-11 years, members return to where they last encountered the corpse the chances are it will have when they are approaching Piaget’s stage of “formal operations” and show increased disappeared, due to a combination of biotic degradation processes and scavengers competence at dealing with abstract concepts (Inhelder and Piaget 1958). A grasp of the feeding on and dispersing it (but see Anderson 1984, for exceptions). biological causes of death is the last component to be acquired, with the others being The situation is different for species that congregate permanently (or semi- understood a few years earlier (Slaughter and Griffiths 2007; Speece and Brent 1984). permanently) at a fixed site, such as nests of social insects. Indeed, it has been Some evidence suggests that children with personal experience of bereavement – suggested that cues to the origins of funerary activities in earlier human societies are resulting from the demise of a family member, for example – have a more mature likely to be found where groups lived in a relatively fixed place (Pettitt 2011). The nests appreciation of irreversibility and non-functionality, along with an enhanced overall and hives of social insects provide another example of where corpse management is understanding of death. Depictions of death in drawings may also differ as a function of important. These enclosed environments, often associated with high population bereavement experience in childhood (Bonoti et al. 2013). densities as well as food reserves, provide ideal conditions for the proliferation of Alongside academic and applied interest in how modern humans deal with death and potentially harmful organisms. If conspecifics die within the nest, the remaining colony dying, some thanatologists embrace evolutionary approaches. For example, palaeontologists members are in potential danger of infection from the decaying corpses. Social insects and physical anthropologists attempt to piece together the emergence and development such as bees, wasps, ants and termites deal with this problem through an evolved suite of corpse disposal practices among prehistoric and later hominids (e.g., Pettitt 2011). of behaviors all of which have the same end result: rapid and effective disposal of dead Biologists and ethologists study other species’ responses to dead and dying individuals conspecifics. Within the colonies, some individuals become specialized “undertakers” from the perspectives of natural selection and underlying biological and psychological whose role is to detect and dispose of dead colony members. López-Riquelme and mechanisms (Anderson 2016; Archer 1999; King 2016). In the remainder of this article I Fanjul-Moles (2013) describe the following four behavioral responses to corpses: 1) review some thanatological research on nonhuman animals, with a particular focus on Necrophoresis is the transport and disposal of corpses either outside of the nest or at behavioral and emotional responses to corpses in nonhuman primates. I then propose a refuse sites within the nest; this is especially typical of social bees and wasps. 2) tentative comparison of some responses to the dead observed in modern humans and in Cannibalism is the consumption dead conspecifics; it is the main corpse disposal our nearest evolutionary neighbors, chimpanzees. My overall aim is to elucidate some mechanism in termites, but is also reported in ants. 3) Burial behaviour refers to commonalities between how humans and nonhumans deal with their dead, and to argue covering corpses with soil or other matter; it appears common especially in termites, that increased knowledge of the impact of the dead on living nonhumans can help our less so in ants. 4) Necrophobia is the simple avoidance of corpses or areas associated understanding of the evolution of modern humans’ concepts of and reactions to death. with corpses, as observed in ants and termites. Each of the four behaviors outlined above represents an adaptive strategy used by social insects to reduce the chance of illness and death arising from infection through 176 James R. Anderson close contact with decaying corpses. A recent study illustrates the effectiveness of corpse removal in colonies of common red ants. Diez et al. (2014) compared survival rates in colonies that were free to remove corpses with colonies in which corpse removal was impeded because the size of the entrance to the nest was experimentally reduced. Following the placement of freshly killed nest-mates in each nest, the numbers of dead and live ants and larvae in the nests were counted over a 7-week period. From the eighth day after corpse placement, adult worker survival rates in colonies with restricted removal possibilities were significantly reduced compared to colonies with normal-size nest entrances. Ants in both treatment conditions made efforts to remove the dead: whereas those in normal-size entrance nests performed typical necrophoric behaviors, those in restricted entrance nests cut up and removed corpses piece by piece. By the end of the study larvae survival rates were also found to be lower in the restricted entrance nests. Additionally, corpses that were not cut up and ejected were moved to areas of the nest as far away from the larvae as possible. Social insects’ efficient corpse disposal strategies have been shown to be innate – or pre-programmed – behavior patterns, triggered by largely chemical cues from the corpses. In a pioneering study, Wilson et al. (1958) identified oleic acid as one of the decomposition-related products that induced necrophoric behavior in ants; they described how any objects that were daubed with this substance were treated like corpses and removed to refuse piles, even live, healthy nest-mates! Notwithstanding inter-species variability in which chemical cues alone or in combination elicit corpse disposal in insects, there is general agreement regarding the role of such “necromones” in eliciting undertaking behavior in social insects (Lopez-Riquelme and Fanjul-Moles 2013). Another significant discovery is that two chemical compounds found in live ants may inhibit inappropriate necrophoric responses by nest-mates due to their masking effect on pre-existing necromones; the rapid fading of such compounds in freshly dead workers may be sufficient to elicit their removal even before necromones take effect (Choe et al. 2009). The purpose of the above foray into entomology is to highlight that what can broadly be described as funerary behaviors have ancient origins that most likely predate any “comparable” behaviors that have evolved in primates. One aspect of responses to death that undoubtedly differs between insects and primates, however, is the underlying psychology (Anderson 2016). Corpse disposal mechanisms of insects adhere to classic ethological sequences of sign stimulus  innate releasing mechanism  fixed action pattern in the absence of any recognizable emotional components. By contrast, not only do responses to dead conspecifics by primates include a spectrum of behaviors ranging from indifference to intense engagement, they are also accompanied by sometimes intense emotional experiences, as discussed below.

James R. Anderson Grief in Nonhuman Animals 177 close contact with decaying corpses. A recent study illustrates the effectiveness of corpse Responses to Death in Nonhuman Primates (and Some Other Species) removal in colonies of common red ants. Diez et al. (2014) compared survival rates in colonies that were free to remove corpses with colonies in which corpse removal was Before focusing on the thanatology of our nearest evolutionary neighbors, the impeded because the size of the entrance to the nest was experimentally reduced. anthropoid primates, it would be remiss not to acknowledge the many interesting and Following the placement of freshly killed nest-mates in each nest, the numbers of dead important observations of death-related responses that have been reported in and live ants and larvae in the nests were counted over a 7-week period. From the nonprimate vertebrate species. Space constraints preclude adequate coverage here, but eighth day after corpse placement, adult worker survival rates in colonies with examples include discovery of the role of the chemical compounds cadaverine and restricted removal possibilities were significantly reduced compared to colonies with putrescine in eliciting burial of dead conspecifics by rats (Pinel et al. 1981), noisy normal-size nest entrances. Ants in both treatment conditions made efforts to remove “cacophonous aggregations” in avian corvids following discovery of a dead conspecific the dead: whereas those in normal-size entrance nests performed typical necrophoric (Iglesias et al. 2012), caretaking and distress reactions of elephants in the presence of a behaviors, those in restricted entrance nests cut up and removed corpses piece by piece. dying and dead adult group member (Douglas-Hamilton et al. 2006), and attention and By the end of the study larvae survival rates were also found to be lower in the caretaking attempts given to dead conspecifics by bottlenose dolphins (Dudzinski et al. restricted entrance nests. Additionally, corpses that were not cut up and ejected were 2003). These and other accounts are essential contributions toward any adequate moved to areas of the nest as far away from the larvae as possible. evolutionary thanatology project, but for the best living models of the impact of the dead Social insects’ efficient corpse disposal strategies have been shown to be innate – or on the living in the earliest humans and pre-human ancestors, we turn to the extant pre-programmed – behavior patterns, triggered by largely chemical cues from the nonhuman primates. corpses. In a pioneering study, Wilson et al. (1958) identified oleic acid as one of the decomposition-related products that induced necrophoric behavior in ants; they Responses to Dead Infants described how any objects that were daubed with this substance were treated like Despite the tens of thousands of hours of observations of nonhuman primates in their corpses and removed to refuse piles, even live, healthy nest-mates! Notwithstanding natural habitats by field researchers, there remain surprisingly few reports of deaths inter-species variability in which chemical cues alone or in combination elicit corpse directly witnessed by researchers, and the responses of conspecifics to the corpse. One disposal in insects, there is general agreement regarding the role of such “necromones” exception to this dearth of information is the phenomenon of carrying and caring for in eliciting undertaking behavior in social insects (Lopez-Riquelme and Fanjul-Moles dead newborn and young infants. Continued attempts to take care of dead infants by 2013). Another significant discovery is that two chemical compounds found in live ants the mother have been reported in the three major groups of primates. Mothers of may inhibit inappropriate necrophoric responses by nest-mates due to their masking prosimian species such as lemurs are less likely to carry dead offspring but show effect on pre-existing necromones; the rapid fading of such compounds in freshly dead interest and some caretaking before abandoning the corpse (Nakamichi et al. 1996). workers may be sufficient to elicit their removal even before necromones take effect Mothers of New World primate species such as squirrel monkeys and capuchin monkeys (Choe et al. 2009). sometimes succeed in picking up and transporting their dead infant, and they examine The purpose of the above foray into entomology is to highlight that what can broadly and touch it (Kaplan 1973; Ramírez-Llorens et al. 2008). The phenomenon appears most be described as funerary behaviors have ancient origins that most likely predate any widespread and observable in Old World monkeys such as baboons and macaques “comparable” behaviors that have evolved in primates. One aspect of responses to death (Altmann 1980; Sugiyama et al. 2009) as well as in African great apes (chimpanzees: that undoubtedly differs between insects and primates, however, is the underlying Biro et al. 2010; van Lawick-Goodall 1968; mountain gorillas: Warren and Williamson psychology (Anderson 2016). Corpse disposal mechanisms of insects adhere to classic 2004). In such cases there may be considerable behavioral adjustment by mothers in ethological sequences of sign stimulus  innate releasing mechanism  fixed action their efforts to continue to transport the lifeless infant, for example by holding the baby pattern in the absence of any recognizable emotional components. By contrast, not only in one hand and walking on three limbs; some monkey mothers have even been seen do responses to dead conspecifics by primates include a spectrum of behaviors ranging holding their dead infant in their mouth during locomotion. The corpse may be kept by from indifference to intense engagement, they are also accompanied by sometimes the mother for hours, days, or many weeks, and retained even when parts of the body intense emotional experiences, as discussed below. become detached due to decomposition or mummification. Maternal behavior towards dead infants is of interest for our understanding of the evolution of the emotional bond between mothers and their offspring, the grief process 178 James R. Anderson in bereavement, and the influence of social and environmental factors on dealing with the dead (Anderson 2016; Fashing et al. 2011; Fashing and Nguyen 2011; Sugiyama et al. 2009). For example, the well documented accounts of depressive reactions – behavioral withdrawal accompanied by physiological changes in primates in response to involuntary and prolonged separations from their primary attachment figures – make it highly likely that bereaved primates experience similar intensely negative emotions following the death of a close relative or companion (Anderson 2016; King 2016) (see below). In several species it is not only the mother who continues to “interact” with a dead infant; other members of the group may approach, investigate, carry, groom and generally look after the corpse. These behaviors may not be restricted to the close family members. In two large groups of semi free-ranging Barbary macaques, males of all ages were seen to handle dead infants in various ways, including protecting them from “danger” and waving away flies. Adult males also used dead infants to facilitate close- distance interactions with other adult males, similar to their way they use live infants (Merz 1978). In some of the cases described in this section the cause of the infant’s death was unknown; in others death followed a period of illness, and in a further subset the infant was killed in an infanticidal attack. It would be interesting to know more about how events leading up to death might differentially influence the behavior of other members of the group towards the corpse. In the longer term these kinds of observations might also be of value for our understanding the origins of differential treatment of corpses of infants and adults in many modern and prehistoric human cultures.

Responses to Traumatic Deaths of Older Individuals, Including Predation Predation is a major cause of mortality in many primate populations, and witnessed predation events also clearly affect the behavior and physiology of survivors. In one region of Botswana, two daytime predatory attacks by lions within 1 km of a baboon sleeping site led to the baboons moving no more than 200 m from the sleeping site the following day. By contrast, in the same locality leopards hunted baboons by climbing into the latters’ sleeping groves at night. Busse (1980) gave little information on the reactions of other members of the group to these nocturnal attacks other than general frenzied activity and scattering in the trees, but a baboon group in Kenya was reported to permanently abandon a sleeping grove after leopards killed two members of the group therein (Altmann and Altmann 1970). In Gombe, Tanzania, over half of immature red colobus monkeys may be killed and eaten by chimpanzees. During hunting episodes by the latter, adult red colobus often attempted to counterattack and sometimes inflicted wounds on the apes. In the aftermath of attacks the surviving monkeys were visibly distressed, but remarkably, the following day they showed no evidence of avoiding the area where a hunt had James R. Anderson Grief in Nonhuman Animals 179 in bereavement, and the influence of social and environmental factors on dealing with previously taken place (Stanford 1998). Gombe chimpanzees also kill and consume the dead (Anderson 2016; Fashing et al. 2011; Fashing and Nguyen 2011; Sugiyama et young baboons. Teleki (1973a) reported that adult baboons noisily harassed al. 2009). For example, the well documented accounts of depressive reactions – chimpanzees who had captured an infant baboon for as long as the latter remained alive, behavioral withdrawal accompanied by physiological changes in primates in response to especially if it was vocalizing and struggling to escape. However, when the captured involuntary and prolonged separations from their primary attachment figures – make it infant died or if it was already dead when adult baboons arrived, the latter quickly highly likely that bereaved primates experience similar intensely negative emotions calmed down and lost interest, and generally left the area within 30 min. Adult females following the death of a close relative or companion (Anderson 2016; King 2016) (see including the infant victim’s mother, however, typically stayed in the vicinity for much below). longer; one mother visited the site alone and wandered around it several hours after the In several species it is not only the mother who continues to “interact” with a dead infant had been eaten. infant; other members of the group may approach, investigate, carry, groom and A final example of the consequences of predation events on victims’ relatives provides generally look after the corpse. These behaviors may not be restricted to the close family evidence for the stressful nature of bereavement in nonhuman primates. As already members. In two large groups of semi free-ranging Barbary macaques, males of all ages mentioned, baboons in the Moremi Game Reserve of Botswana are targets of predatory were seen to handle dead infants in various ways, including protecting them from leopards and lions. Based on analysis of stress hormones extracted from faeces, Engh et “danger” and waving away flies. Adult males also used dead infants to facilitate close- al. (2006) reported significant stress hormone elevations in female baboons who had distance interactions with other adult males, similar to their way they use live infants recently lost a close relative to a predator, but not in unrelated females, even though (Merz 1978). In some of the cases described in this section the cause of the infant’s the latter also witnessed the predatory attacks. Another interesting aspect of this study death was unknown; in others death followed a period of illness, and in a further subset is that by engaging in bouts of social grooming with a greater number of partners than the infant was killed in an infanticidal attack. It would be interesting to know more before the predatory event, bereaved females’ physiological states gradually returned to about how events leading up to death might differentially influence the behavior of normal. This research strongly suggests that grief is likely to characterize not only other members of the group towards the corpse. In the longer term these kinds of recently bereaved mothers (and possibly siblings) of dead infants as described above, observations might also be of value for our understanding the origins of differential but also close relatives and friends of older individuals who die traumatically within the treatment of corpses of infants and adults in many modern and prehistoric human group. cultures. In most cases of predation the victim is eaten by the predator, so other group members have no chance to respond directly to the corpse. But why are there so few Responses to Traumatic Deaths of Older Individuals, Including Predation observations of responses to corpses of older nonhuman primates that have not been Predation is a major cause of mortality in many primate populations, and witnessed killed by predators? There are several reasons (Anderson 2011). In captivity, terminally predation events also clearly affect the behavior and physiology of survivors. In one ill or severely injured individuals are usually removed from their social group and region of Botswana, two daytime predatory attacks by lions within 1 km of a baboon euthanized away from their group-members. In the wild, individuals who are visibly sleeping site led to the baboons moving no more than 200 m from the sleeping site the injured or ill often simply disappear: they are seen by observers one day, but with no following day. By contrast, in the same locality leopards hunted baboons by climbing further sightings after the observers make contact with the group again the following into the latters’ sleeping groves at night. Busse (1980) gave little information on the day. The typical and probably correct assumption in such cases is that the moribund reactions of other members of the group to these nocturnal attacks other than general individual has crawled away to die in a secluded or concealed location, or predators frenzied activity and scattering in the trees, but a baboon group in Kenya was reported have finished the individual off at some point during the night. In either case, no direct to permanently abandon a sleeping grove after leopards killed two members of the responses to the corpse by the dead individual’s group members are witnessed. group therein (Altmann and Altmann 1970). Two interesting cases of responses to sudden, traumatic deaths in wild chimpanzees In Gombe, Tanzania, over half of immature red colobus monkeys may be killed and are worth describing. The precise moment of death was not observed, but reactions eaten by chimpanzees. During hunting episodes by the latter, adult red colobus often shortly thereafter were. At Gombe, Tanzania, Teleki (1973b) discovered a group of 16 attempted to counterattack and sometimes inflicted wounds on the apes. In the chimpanzees erupting into “frenzied activity and raucous calling” (p. 84). Several adult aftermath of attacks the surviving monkeys were visibly distressed, but remarkably, males engaged in aggressive displays that included stamping on the ground, tearing the following day they showed no evidence of avoiding the area where a hunt had and dragging vegetation and throwing stones in various directions. Individuals 180 James R. Anderson frequently paused from their highly excited and noisy activities to look down at the cause of the excitement: the body of an adult male who had just fallen out of a tree and broken his neck (confirmed by necropsy). During the general frenzy some individuals embraced, mounted and touched each other while showing facial expressions of fear and disquiet. After almost 10 minutes the excitement abated, with individuals gazing at the corpse from various distances, and occasional vocalizing. Some displayed again after peering at the corpse. At least 12 individuals congregated around the corpse and mostly gazed at it in silence, but none physically contacted it. Approximately 10 minutes later, some individuals started to groom and eat, as interest in the corpse continued to wane. Occasional vocalizations, charging displays, and copulations occurred over the following half-hour, after which several individuals moved away from the corpse and climbed into trees from where they could still look at it. After another 2.5 h the chimpanzees gradually left the area, some doing so after a long final look towards the corpse. Reactions to another sudden, traumatic death were observed in a group of chimpanzees in the Taï Forest, Ivory Coast. Boesch and Boesch-Achermann (2000) report that a leopard attacked and killed an adolescent female before probably being chased away by an adult male chimpanzee. When the authors arrived on the scene 12 adult chimpanzees were sitting quietly near the body, which had several open wounds. Some males began displaying aggressively and dragged the corpse short distances along the ground. One adult male then inspected and held one of the dead female’s hands, and others started to groom her. Adult females approached and smelled the corpse, but with the exception of the dead female’s young brother any infants who approached were chased away. Different adult males touched the dead female’s chin or gently shook one of her limbs while looking at her face. The brother also groomed her and gently pulled her hand while looking at her face. After a couple of hours increasing numbers of flies landed on the corpse and laid eggs in the nose, eyes, and wounds. The adult chimpanzees waved the flies away and removed the eggs, occasionally returning to the body to do so after they had moved away. The last chimpanzee to abandon the body did so more than six hours after the fatal attack. The two cases outlined above raise many questions about how chimpanzees perceived the death of their group-member. In the first case no individuals touched the corpse, whereas in the second case the corpse was dragged over the ground, manipulated, and groomed. What are the reasons for this difference? Is the age- and sex-class of the dead individual a factor in how others respond? Does social status (of both the deceased and the survivors) play a role? Is cause of death a determinant of how others respond to the body? Why were infants except for the dead female’ young brother kept away from the body? Chimpanzees manifest cultural variations in many aspects of their behavior (McGrew 2004; Whiten et al. 1999); might death-related reactions also show cultural variations? James R. Anderson Grief in Nonhuman Animals 181 frequently paused from their highly excited and noisy activities to look down at the In both cases described above the initial reactions to the fatal incident included noisy cause of the excitement: the body of an adult male who had just fallen out of a tree and and frenzied excitement, eventually followed by quieter activities around the corpse. A broken his neck (confirmed by necropsy). During the general frenzy some individuals final case study, presented below, reveals some similarities and differences with those embraced, mounted and touched each other while showing facial expressions of fear and two accounts, and gives further insights into the emotional consequences of disquiet. After almost 10 minutes the excitement abated, with individuals gazing at the bereavement in chimpanzees. corpse from various distances, and occasional vocalizing. Some displayed again after peering at the corpse. At least 12 individuals congregated around the corpse and mostly The Peaceful Death of an Old Female Chimpanzee gazed at it in silence, but none physically contacted it. Approximately 10 minutes later, Anderson et al. (2010) described events surrounding the death of an old female some individuals started to groom and eat, as interest in the corpse continued to wane. (“Pansy”) in a small captive group of chimpanzees in a safari park in Scotland. Pansy Occasional vocalizations, charging displays, and copulations occurred over the following (estimated to be 55 years old age) lived with her lifelong female friend (“Blossom,” 50 half-hour, after which several individuals moved away from the corpse and climbed into years), her adult daughter (“Rosie,” 20 years old) and an adult male (“Chippy,” 20 years trees from where they could still look at it. After another 2.5 h the chimpanzees old, Blossom’s son). In November 2008 caretakers noticed an increasingly lethargic gradually left the area, some doing so after a long final look towards the corpse. Pansy spending unusually long periods of time lying on the ground on their small island, Reactions to another sudden, traumatic death were observed in a group of even in cold temperatures. When the chimpanzees were eventually transferred to their chimpanzees in the Taï Forest, Ivory Coast. Boesch and Boesch-Achermann (2000) warm indoor winter quarters, Pansy mostly continued to lie on the straw covered floor, report that a leopard attacked and killed an adolescent female before probably being where she was frequently attended to and groomed by the others, who appeared quieter chased away by an adult male chimpanzee. When the authors arrived on the scene 12 than normal. For several days the three healthy chimpanzees were temporarily held in adult chimpanzees were sitting quietly near the body, which had several open wounds. an adjacent room during the daytime while Pansy received medication, food, and liquids. Some males began displaying aggressively and dragged the corpse short distances along Blossom, Rosie and Chippy were allowed to join Pansy each night. Notably, instead of the ground. One adult male then inspected and held one of the dead female’s hands, and making night nests on elevated platforms as they usually did, they made nests on the others started to groom her. Adult females approached and smelled the corpse, but with ground, next to Pansy who appeared too weak to climb up to the platforms. the exception of the dead female’s young brother any infants who approached were On December 7th, the head caretaker noticed a serious deterioration in Pansy’s chased away. Different adult males touched the dead female’s chin or gently shook one condition. Having clambered onto a platform, she got up and moved unsteadily across to of her limbs while looking at her face. The brother also groomed her and gently pulled the other platform, where she lay down in the nest that her daughter had made the her hand while looking at her face. After a couple of hours increasing numbers of flies previous night. About one hour later her breathing became erratic and laborious. landed on the corpse and laid eggs in the nose, eyes, and wounds. The adult Anticipating that Pansy would soon die, the caretaker decided to allow the other chimpanzees waved the flies away and removed the eggs, occasionally returning to the chimpanzees to join her and to leave the group undisturbed. Video cameras recorded the body to do so after they had moved away. The last chimpanzee to abandon the body did scene. so more than six hours after the fatal attack. Figure 1 shows that in the 10 minutes before Pansy died she received 11 instances of The two cases outlined above raise many questions about how chimpanzees perceived grooming or caressing by other chimpanzees, and zero instances in the 10 minutes after the death of their group-member. In the first case no individuals touched the corpse, she died, which was presumed to be at 16:24. At this point Chippy joined the two whereas in the second case the corpse was dragged over the ground, manipulated, and females who were already grooming and stroking Pansy. Chippy peered closely at groomed. What are the reasons for this difference? Is the age- and sex-class of the dead Pansy’s face and gently pulled at her left shoulder and arm, then appeared to touch her individual a factor in how others respond? Does social status (of both the deceased and mouth. All three chimpanzees looked closely at Pansy’s face, which Chippy manipulated the survivors) play a role? Is cause of death a determinant of how others respond to the before again shaking her left shoulder and arm. At 16:25 Chippy and Rosie both moved body? Why were infants except for the dead female’ young brother kept away from the away; Blossom remained for another 25 sec, stroking Pansy’s hand and then just sitting body? Chimpanzees manifest cultural variations in many aspects of their behavior quietly, before also leaving. (McGrew 2004; Whiten et al. 1999); might death-related reactions also show cultural The video cameras continued to record throughout the night, after the main lights variations? went off at 16:36. Within a minute of the lights going off, Chippy performed an aggressive charging display in which he jumped onto the platform where Pansy’s body 182 James R. Anderson

Figure 1: Frequency of affiliative contacts toward Pansy in the period from 10 minutes before her death until 10 minutes after death. lay and jumped onto the body, pounding it with both hands before running away. Two similar displays occurred the following morning: one at 08:42 after which Chippy sat down and removed straw from Pansy’s back, and at 08:51, after which he leaned forward and looked closely at Pansy before moving calmly away. A few minutes before the first morning display by Chippy, Blossom came to Pansy and brushed away straw that covered from her body and face/neck as a result of Chippy’s display the previous night. Between the evening and morning displays by Chippy, several other aspects of the three surviving chimpanzees’ behavior stood out. Figure 2 illustrates their nighttime locations: on the leftmost platform lay Pansy’s body, with Rosie lying nearby, facing away from the body. That night Rosie made her nest in an area of the platform where she had never been seen to nest previously, and she did this much later than normal. On the second platform Blossom lay near to Chippy, grooming him considerably more than she normally did at nighttime. All three chimpanzees showed unusually disrupted sleep, making many more postural changes (Rosie: 11, Chippy, 15, Blossom: 42) than the usual 4 or 5 shifts per night (see Fig. 2). The following morning the caretakers noted that all three surviving chimpanzees appeared subdued. From an adjacent room they watched silently while two caretakers removed Pansy’s body from the platform and then the building. Their depressed James R. Anderson Grief in Nonhuman Animals 183

Positions of the four chimpanzees on the two elevated platforms during the night

following Pansy’s death.

Figure 2: Average frequency of nightly postural changes recorded during a 1-month study Figure 1: Frequency of affiliative contacts toward Pansy in the period from 10 minutes in the previous year (PY), and total number of postural changes during the night before her death until 10 minutes after death. of Pansy’s death (ND). lay and jumped onto the body, pounding it with both hands before running away. Two demeanor continued after the indoor quarters were cleaned and new straw was similar displays occurred the following morning: one at 08:42 after which Chippy sat provided. The two females moved into the newly prepared quarters hesitantly, but the down and removed straw from Pansy’s back, and at 08:51, after which he leaned male showed some fear reactions and for two days he refused to enter the area where forward and looked closely at Pansy before moving calmly away. A few minutes before Pansy had died. When the three chimpanzees did resume sleeping on an elevated the first morning display by Chippy, Blossom came to Pansy and brushed away straw platform, for five consecutive nights none of them made their nest on the platform that covered from her body and face/neck as a result of Chippy’s display the previous where Pansy had died; a very unusual occurrence. night. With the exception of the three attacks by the adult male on the corpse, the responses Between the evening and morning displays by Chippy, several other aspects of the of the three chimpanzees to the progressively ailing and dying old female chimpanzee three surviving chimpanzees’ behavior stood out. Figure 2 illustrates their nighttime contrast in several ways with those recorded in response to traumatic deaths in the wild. locations: on the leftmost platform lay Pansy’s body, with Rosie lying nearby, facing Before she died the others were quiet and attentive towards her, and they changed their away from the body. That night Rosie made her nest in an area of the platform where normal routine by making their night nests beside her on the ground instead of on the she had never been seen to nest previously, and she did this much later than normal. elevated platforms. As Pansy died the other chimpanzees looked closely at her face, On the second platform Blossom lay near to Chippy, grooming him considerably more with manipulation and gentle shaking of her body (also reported by Boesch and Boesch- than she normally did at nighttime. All three chimpanzees showed unusually disrupted Achermann 2000). For the first time, we were able to record chimpanzees’ behavior in sleep, making many more postural changes (Rosie: 11, Chippy, 15, Blossom: 42) than the vicinity of a dead group-member during the night. After the immediate reactions to the usual 4 or 5 shifts per night (see Fig. 2). the death and the first attack by the adult male, the dead female’s daughter remained The following morning the caretakers noted that all three surviving chimpanzees close to her mother’s body all night (though she made no contact, and rarely appeared to appeared subdued. From an adjacent room they watched silently while two caretakers even look at the body), while affiliative behavior (grooming) between the other removed Pansy’s body from the platform and then the building. Their depressed individuals increased. Sleep was clearly disturbed. Two individuals removed straw from 184 James R. Anderson

Chimpanzees Humans Before death: Quiet, attentive, Care, respect modified sleeping arrangements anticipatory grief

Around time of death: Inspection of mouth, move Check for breathing and shake body, limbs or for pulse

Aggression: attempt to Attempted resuscitation rouse the body? After death Remain in proximity to body Night-time vigil for deceased

Frequent postural changes Disturbed sleep during the night

Increased grooming Consolation; social and emotional support

Aggression: anger or Denial, feelings of anger frustration?

Lethargy, lower activity, Grief, depression loss of appetite

Avoidance of sleeping on Leaving deceased’s objects or deathbed platform spaces untouched (For human behaviors see Blinderman and Billings 2015; Kübler-Ross 1969; Parkes et al. 1997; Stewart 2003; Sweeting and Gilhooly 1990). Table 1. Behaviors in response to dying and dead individuals in chimpanzees (observed by

Anderson et al. 2010) and humans. the body the following morning, and for five nights all three avoided sleeping near to where the female had died. For several weeks after the death all three chimpanzees showed subdued activity levels and reduced appetite, before gradually returning to normal. Until further observations on death-related reactions accumulate from wild populations as well as those in captivity, we cannot draw conclusions about possible reasons for the contrasting reactions described above. For example, living permanently together in captivity meant that the old female’s group members were able to witness her gradually failing physical health and were present as her death became imminent. In the natural habitat, by contrast, the fission-fusion system of chimpanzees means that individuals may not see particular individuals of their community for extended periods, and so may be unaware of others’ illnesses or injuries. Similarly, it seems likely that the traumatic deaths in the wild might have induced generalized fear responses in other group members that did not occur in the context of the old female’s peaceful death. Of course, as indicated earlier, it also seems likely that responses to death might be influenced by cultural factors in great ape populations.

James R. Anderson Grief in Nonhuman Animals 185

Conclusions

Table 1 lists some of the phenomena observed in the case of Pansy’s death in a close- knit group of chimpanzees, and some behaviors commonly seen in human responses to the late stages of the life of a terminally ill family member or friend, including after death (Blinderman and Billings 2015; Kübler-Ross 1969; Parkes et al. 1997; Stewart 2003; Sweeting and Gilhooly 1990). New information on how nonhuman primate species deal with dead and dying group-members is rapidly accumulating (see Bezzera et al. 2014; Buhl et al. 2012; Stewart et al. 2012; Van Leeuwen et al. 2016; Yang et al. 2016); the currently available literature appears sufficiently solid to allow at least two conclusions. First, nonhuman primates experience distress and can become depressed after the death of a bonded individual such as kin or a close partner. Reports of responses to deaths by surviving mothers, siblings, and even friends within primate communities have long suggested human-like grief reactions (e.g., Goodall 1971), but researchers now have more objective supporting measures. Second, along with their grief reactions, survivors’ experiences of non-responsiveness, lack of agency, and the permanence of the changes in dead individuals suggests that they might well be capable of understanding two of the elements of the human concept of death, namely Table 1. Behaviors in response to dying and dead individuals in chimpanzees (observed by irreversibility and non-functionality. In humans, starting from childhood culture Anderson et al. 2010) and humans. massively influences how dying and dead individuals are treated (Lobar et al. 2006; Parkes et al. 1997); religious belief is one aspect of culture that clearly differentiates the body the following morning, and for five nights all three avoided sleeping near to humans from nonhuman primates. Primatologists interested in psychology continue to where the female had died. For several weeks after the death all three chimpanzees work towards clarifying the mental abilities of great apes and other primates compared showed subdued activity levels and reduced appetite, before gradually returning to to those of human adults and children, for example in the domains of self-awareness normal. (Anderson and Gallup 2011; Gallup et al. 2011), theory of mind (Krupenye et al. 2016) Until further observations on death-related reactions accumulate from wild and culture (Gruber et al. 2015; Whiten 2015). Future observations from such fields of populations as well as those in captivity, we cannot draw conclusions about possible enquiry may help to clarify which death-related behaviors in Table 1 are analogous and reasons for the contrasting reactions described above. For example, living permanently which are homologous across species. What appears undeniable, however, is that at together in captivity meant that the old female’s group members were able to witness least some core human ways of responding to death and bereavement have their roots her gradually failing physical health and were present as her death became imminent. in our long, shared evolutionary past with other primates. In the natural habitat, by contrast, the fission-fusion system of chimpanzees means that individuals may not see particular individuals of their community for extended periods, and so may be unaware of others’ illnesses or injuries. Similarly, it seems likely that the traumatic deaths in the wild might have induced generalized fear responses in other group members that did not occur in the context of the old female’s peaceful death. Of course, as indicated earlier, it also seems likely that responses to death might be influenced by cultural factors in great ape populations.

186 James R. Anderson

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