Nonhuman Reactions to Death
KeywordsNonhuman Animal Dead Body Intergroup Encounter Dead Infant Adult Male Chimpanzee
Death – The action or fact of dying or being killed; the point at which the processes that maintain an organism alive no longer function. Dead – Deprived of life; opposed to alive and living; reduced to that state of a being in which the organs of motion and life have irrevocably ceased to perform their functions.
Awareness of mortality is a human universal, evidenced by the pervasiveness of mortuary behavior and funerary rituals across human cultures, dating to Neanderthals over 40 ka. Humans exhibit diverse cultural variation in mortuary practices, in which treatment of dead bodies ranges from their consumption to the placement of them as far above or below ground as possible (Andrews et al. 2006). Moreover, compassionate behavior toward dying individuals is often regarded as a uniquely human trait, though recent reports of reactions to death and dying in nonhuman animals highlight the value of adopting a comparative evolutionary approach toward these behaviors. Here the diversity of nonhuman animal responses to death is reviewed and explanations for why animals differ so widely in their behavior toward dead conspecifics suggested.
Diversity of Responses to Death
Behavioral Adjustment to a Risk Exposure
If animal responses to carcasses are adaptive, individuals would be expected to view the bodies of dead conspecifics as disease-carrying agents and avoid or isolate them accordingly. Ants and aphids do exactly this, carrying carcasses to refuse piles, while honey bees remove dead brood members from their hives. Rats bury decomposing den mates. Nonetheless, there is information to be gleaned from dead or dying conspecifics, especially in assessing potential risk in an area. In some birds, seeing a dead conspecific induces alarm calling and subsequent risk-reducing behavior (Swift and Marzluff 2015), while in many aquatic organisms (Phylum Protista, Rotifera, Mollusca, Arthropoda, and Chordata), chemical cues perceived from injured, dead, or digested conspecifics results in complete aversion to the local area.
Intense Interest in Conspecific Carcasses
Alternatively, some animals show intense interest in conspecific carcasses. In perhaps the best known example, African elephants spend unusually long periods at the sites where former herd members’ bodies lie decomposing or even where only bones remain. They may also exhibit intense agitation and investigation (Merte et al. 2008). Less known, although behaviorally similar, American bison chase wolves away, before sniffing and nuzzling a calf’s rotting body from their herd (King 2013). A similar reaction was reported by Strauss and Muller (2012) in wild giraffes, where following the death of a calf, giraffe mothers, and other herd members exhibited prolonged interest, including extensive vigilance, nuzzling, sniffing, and inspection of the carcass over several days. Intense interest in conspecific carcasses was also observed for a variety of cetaceans (i.e., rough-toothed dolphins, bottle nosed dolphins, Orca). The described behaviors include staying beside injured, dying, or net-trapped conspecifics and supporting sick or dead animals (infant as well as adult) at the surface (Ritter 2007).
Infant Corpse Carrying
Evolutionary biology predicts the extensive interest mothers’ exhibit in dead offspring. Mammals that experience long gestation and development will benefit with the successful survival (and subsequent reproduction) of their offspring, thus premature abandonment of a suffering, but viable offspring carries high fitness costs. Examples of responses to dead infants date from almost a half-century ago and seem concentrated in the Order Primates. In numerous species, mothers and other group members carry dead infants from a few days up to several months after their death. Recently, Li et al. (2012) described three cases of mother responses toward dead infants in Yunnan snub-nosed monkeys. They showed that the age at which the infant died influenced the mother’s behavior, whereby, for example, there was no carrying of stillborns versus extensive carrying of dead infants who had survived to at least 1 month. Given that nonhuman primate females are hormonally predisposed to mothering in the last weeks of pregnancy, it is likely that hormones associated with parturition and lactation combined with the formation of a strong mother–infant attachment offer the strongest explanation for these behaviors. Between adults, the pre-dead relationship between the dead and the survivor seems to play an important role. Individuals that are more closely affiliated with the dead exhibit stronger reactions, either immediately or through longer-term behavioral changes. Given the importance of relationships to social animals, from alliance formation in dominance takeovers to cooperative foraging strategies, the loss of an ally can generate tremendous survival cost.
Sexual Arousal and Aggressive Interactions
If removing or isolating a carcass from one’s home base makes adaptive sense by reducing potential exposure to disease, spending significant time investigating dead bodies seems maladaptive. However, sociosexual interactions with carcasses appear in several species (Piel and Stewart 2016). In marine mammals, Dudzinski and colleagues (2003) reported six to eight male dolphins spending almost three hours with a female carcass, focusing almost all their attention on its genital area, and simultaneously mate guarding the carcass while aroused. Similarly, mallards were observed to display homosexual and necrophilic behavior toward dead conspecifics, and in one anecdotal observation, a male squirrel was seen to approach and lay down in a copulatory posture next to a dead female. Stewart et al. (2012) detailed the responses of 16 (different) chimpanzees to the recently dead body of an adult female community member in Tanzania. Responses ranged from curious observation and passive investigation (e.g., smelling and grooming) to the shaking, dragging, and frustrated beating of the body. Similar responses were described in a nearby community, where adult male chimpanzees use the bodies of dead members in charging displays. Combined, these behaviors reveal a suite of responses, but they share individuals having increased arousal levels, and possible confusion at the lack of response and overall state of the dead individual.
Human-Like Grieving in Captive Animals
One of the human universals in responses to death includes people grieving the loss of group members. This is a response to the permanent absence of the individual (e.g., death) versus the examples above, which describe responses to a dead body. Grief can be defined as changes in the survivor’s patterns of social behavior, eating, sleeping, and/or of expression of affect (King 2013). While it is both difficult to define and rare to observe, there are documented cases of humanlike “grieving” among nonhuman animals. In captive pottos (Perodicticus potto), two individuals who survived a dead cage mate reduced their food intake after the death (and removal) of the conspecific. Captivity, however, allows surviving individuals to adjust their behavior at no cost to their survival. In the wild, natural selection may work against the visible expression of grief, since changes to routine and behavior may make an individual more vulnerable to predation or other lethal aggression from group members.
In perhaps the best description of a sequence of behaviors that approached human grieving, Anderson et al. (2011) reported on the death of an adult chimpanzee at Blair Drummond Safari Park, Scotland. Unique to this report were the detailed video records made before, during, and after the death. The authors described behaviors analogous to those that humans exhibit: chimpanzees appeared to care for the individual before death, to test for signs of life at the point of death, and to show signs of frustration after death, as well as subsequently to avoid the place where the death occurred (after the body was removed). The contrast in behavior pre-, during, and post-death seen in Anderson et al.’s study encouraged the authors to draw conclusions about the possible mental and emotional state of the surviving chimpanzees, specifically whether empathy and self-awareness – traits shared by humans and chimpanzees – allow us also to share with them an awareness of mortality.
What hampers our attempt to understand a nonhuman concept of death is similar to challenges facing any study of nonhuman cognition: How to know what others, unlike ourselves, know? Despite similar neuroanatomy, for example, humans and other primates exhibit vastly different capacities. Thus, it is both anthropocentric and biologically unfounded to expect nonhumans to express rituals as humans do, to communicate and express emotion as humans do. Thus, what can be expected? Besides against that of humans, against what baseline can others’ responses to dead group members be compared? Until objective criteria are provided, analysis is limited by a species-specific lens, preventing much beyond a speculative interpretation of responses to death in heterospecifics.
The question of which species conceptualize death and how that is reified has implications for the evolution of human cognition and ritual. Fear of death has been argued to be a human universal. Full self-awareness and a theory of mind were likely propagated by positive natural selection and in some way must have benefitted ancestral hominins, opening the path for a distinction of “death” from “the dead.” Others have argued to the contrary that these same traits may actually be evolutionarily detrimental to an individual or species. They would be a dead-end evolutionary barrier and would inhibit positively selected behaviors with large payoffs, like risk. Accordingly, a hominoid conception of death might have been blocked at some point during Great Ape evolution, helping to explain how animals can engage in fatal intergroup encounters, for example. Why then do some animals act as if they understand death? Elephants and other large herbivores investigate the bones of dead conspecifics; primate mothers carry dead infants for weeks or months; and, at least in captivity, animal responses to the dead resemble human grief with remarkable similarity.
If corpse removal from a fixed home base by colony-dwelling insects can be explained as an innate, evolutionary behavior, intense interest in conspecific bodies may invoke more complex behaviors not as well known to scientists. Behavior associated with extensive vigilance, or high sexual or aggressive arousal, is presumably exhibited in an effort to gather more information about the unusual unresponsiveness of a carcass and demand more complex cognition, although not necessarily a conception of death. Elephant, giraffe, dolphin, and primates share large complex brains and fluid, complex social organizations that are cognitively demanding. It could be that the same faculties demanded to be a member of these groups are similarly useful in creating an awareness of one’s position in the group and, in turn, the loss of others.
It is impossible to determine whether any of the animals described above have evolved or, more interestingly, developed an awareness or concept of death; only with concrete attempts to define expectations, look for patterns across anecdotes, and, eventually, test hypotheses can this this topic be approached as a scientific question, grappling with the age-old question of human uniqueness.
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