a primatological perspective on death_j.anderson

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American Journal of Primatology 71:15 (2011)

COMMENTARY

A Primatological Perspective on Death

JAMES R. ANDERSON

Department of Psychology, University of Stirling, Stirling, Scotland

Some questions that arise from observations of responses to dead and dying individuals by nonhumanprimates are discussed, focusing on psychological issues. The phenomenon of transport and care of deadinfants is reviewed, along with the consequences of the mother dying for orphaned offspring. It isargued that particular attention should be paid to how the context of a death affects individuals, forexample, traumatic accidental or predation-induced death versus peaceful death following illness. Someprimates kill others of their own or other species, which raises additional questions about deathawareness and empathy. Observations from both the field and captivity can contribute toward a betterunderstanding of the psychological meaning of death for primates. Some aspects of death awareness

recognized by developmental psychologists might help guide research efforts in this area. Am. J.Primatol. 71:15, 2011. r 2011 Wiley-Liss, Inc.

Key words: thanatology; death awareness; dying; predation; bereavement; primates

INTRODUCTION

There are many definitions of thanatology, withdifferent opinions about whether the study of deathand dying in nonhuman species should be included inthe discipline. For some, thanatology is the study of

how humans, and only humans, respond to death;the view taken here is that this is overly restrictive.The study of the impact of death on the behavior ofothers can give valuable insights into psychologicaland social adaptations in a wide range of species,including nonhuman primates [Barrett, 2005; Zeller,1991]. Furthermore, a primatological perspective ondeath and dying is relevant for understanding howaspects of human responses to death might haveevolved. Although primatologists have long acknowl-edged the importance of death (often assumed in thecase of disappearances) for calculations of demo-graphic trends and constructing life tables [e.g.,

Altmann & Altmann, 1970], there are relatively fewstudies that focus on psychological aspects of deathin nonhuman primates. It is this latter aspect thatwill be addressed here.

DEAD INFANTS AND ORPHANS

The paper by Fashing et al. [2010] is a goodstarting point for exploring responses to death innonhuman primates. In the course of nearly 4 yearsof observations on a population of wild geladas inEthiopia, 14 cases were recorded of dead infantsbeing carried by females. Data on a subset of infantsindicated an age range at death of 1180 days, and

postdeath carrying durations of 1 to 448 days(usually not more than 4 days). Attraction towarddead infants was not restricted to the infantsmothers; juvenile females also carried and groomedthem, and even females from another group wereobserved to do so. This appears to be the firstdescription of allomaternal-like behavior toward adead infant from another group, and it raises severalquestions. For example, what was the cause of death?How did an extra-group female obtain the corpsefrom the mother (the transfer took place at thegeladas sleeping cliff)? What was her underlyingmotivation? What was the mothers reaction? Similarquestions arise when considering the responses todead infants by adult males in semi-free-rangingBarbary macaques [Merz, 1978]; males transportedand groomed infant corpses, and used them in so-called agonistic buffering episodes with othermales. Unfortunately, insufficient information is

available for systematic comparison of this behaviorwith its equivalent using live infants.

Fashing et al. [2010] propose that prolongedcarrying of dead infants (defined as longer than10 days) may be more likely in relatively extreme

Published online in Wiley Online Library (wileyonlinelibrary.com).DOI 10.1002/ajp.20922

Received 1 November 2010; revised 9 December 2010; revisionaccepted 10 December 2010

Correspondence to: James R. Anderson, Department ofPsychology, University of Stirling, Stirling FK9 4LA, Scotland.E-mail: [email protected]

2011 Wiley-Liss, Inc.


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climatic conditions, as particularly cold or hot anddry weather may slow the decomposition of corpses.The authors suggest that this might account forsimilar published cases in populations of Japanesemacaques, mountain gorillas, and chimpanzees. By

extension, it could also help explain the phenomenonsrelative rarity in tropical rainforest guenons [e.g.Booth, 1962] and other primates in less climaticallyextreme regions. Compared to Old World primates,New World monkeys appear to carry or care for deadinfants rarely or only for a short time [but seeRumbaugh, 1965 for a prolonged case in captivesquirrel monkeys]. The mother of a wild 2-day-oldtufted capuchin infant no longer had her infantscorpse the morning after the infanticidal attack thatresulted in its death [Izar et al., 2007]. Perry andManson [2008] report a similar case in white-facedcapuchins; they also describe a mother carrying astillborn infant for more than one day in spite of

getting stung by carnivorous wasps that came toforage on it. Although she groomed and licked thebody and tried to prevent insects from getting at it,other aspects of the mothers behavior suggestedsome awareness that the baby was not alive; forexample, she allowed it to be fully submerged inwater while she drank. These cases all raise the issueof death awareness in nonhuman primates.

Another ecological factor that might influencedead infant carrying is arboreality; a lifeless babythat falls to the ground from a great height may beless likely to be retrieved than one that the mother(or another individual) has placed on the ground.

Within- and across-species comparisons in a range ofecological settings would fill in many gaps in ourknowledge about responses to dead infants. Theresulting information could help clarify whethersocial facilitation or cultural transmission play anyrole in cases of prolonged transport of dead infants[see Biro et al., 2010]. The fact that continuedattraction and care toward dead infants occurs tosome extent in all the major taxonomic groupssuggests a phylogenetically old origin; although theyare less able to carry them, prosimian mothers alsoshow affectional behaviors before eventually aban-doning their dead offspring [Nakamichi et al., 1996].

Sometimes adult females peacefully die or get

killed, leaving their immature offspring with theproblem of how to survive without maternal nurturingand protection. Experimental studies of prolongedinvoluntary motherinfant separations in captiveprimates have documented a two-phase reaction,consisting of initial agitation as the infant expressesbehaviors aimed at re-establishing contact with itsmissing attachment figure, followed by a low-activityphase which has been described as similar to a stateof clinical depression. In one well-documented casefrom Gombe, following the death of his mother anadolescent male chimpanzee fell into a deep depres-sive state, culminating in his death three weeks later

[Goodall, 1977]. Although adoptions sometimes occur[Thierry & Anderson, 1986], in general the outlookfor recently orphaned dependent offspring is notgood. In some cases the orphaned infants declineappears directly linked to the perceived loss of the

attachment figure (in captive studies, for example),whereas in others (in free-ranging settings) it is morelikely a consequence of lack of nourishment orwarmth/protection. Fashing et al.s [2010] descrip-tion of the short survival of a 7-month-old geladashe died beside her mothers corpse the followingnightillustrates the latter.

ON CONTEXTS OF DEATH

The circumstances of an individuals deathaffect how others respond to the event and to thecorpse. For example, a stillborn baby or a younginfant dying from disease receives different treat-

ment than one who is killed in an infanticidal attack.As examples of reactions at different extremes of acontinuum, compare prolonged transport and atten-tion to chimpanzee infants who died following illness[Biro et al., 2010] with the killing and consumptionof infants by cannibalistic conspecifics [Goodall,1977; Hamai et al., 1992]. The behaviors of themother (who typically tries to defend her live infantfrom infanticidal attacks) and others are quitedifferent in the two cases. Further study andsystematic comparisons of such cases could help toelucidate the apes perception of death.

The importance of context emerges most clearly

when considering responses to traumatic versuspeaceful death. At Gombe, when an adult male diedinstantly from a broken neck after falling from atree, the other chimpanzees in the party erupted intoa frenzy of alarm calling, displaying, and mutualembracing [Teleki, 1973a]. They gradually quietenedand groomed each other and occasionally inspectedthe body, but without touching it, before they finallyabandoned it several hours later. In the Ta Forest, afatal leopard attack on an adolescent female chim-panzee also caused an outburst of loud calling andaggressive displays by males, who initially draggedthe body over short distances. Unlike at Gombe,contacts with the body were frequent, including

grooming and some gentle shaking. Interestingly,infants were prevented from approaching the body[Boesch & Boesch-Achermann, 2000]. Again, afterseveral hours the corpse was abandoned. These casescontrast sharply with a recently described case incaptive chimpanzees. In a safari park in Scotland,shortly before an elderly female chimpanzee diedfollowing a period of illness, the other members ofher group were especially affiliative toward her. Asshe died the others gathered closely around her andpeered at her face. The adult male lifted her headand shoulders and gently shook her, as if trying toelicit a response (see also the Ta example above).

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Except for an aggressive display directed toward thebody shortly afterwards, the surviving chimpanzeesremained calm and silent, although perturbed,throughout the night, with the deceased femalesadult daughter remaining close by the corpse

[Anderson et al., 2010].The three cases of death and the effects on otherchimpanzees described above are very different,prompting several questions. For example, how doesthe age, sex, or social status (rank) of the deceasedindividual influence how others respond? How doesthe manner in which the individual dies affect theothers immediate responses? Do nonhuman pri-mates anticipate the imminent demise of a seriouslyill group-member? For example, Veit [1982/1998]describes a subordinate silverback male in a group ofwild mountain gorillas as beating up, and therebyhastening the death of, an old and sick female group-member. This eventually led to the silverback over-

throwing the dominant male, who had failed tointervene during the aggressive episode. The authorspeculates that the absence of future reproductivepotential in the old female was a factor in theoverthrown males lack of protectiveness. Finally,why are young infants sometimes prevented fromapproaching a corpse? Only careful observations ofevents surrounding deaths in a range of contexts canstart to provide adequate answers to such questions.

PREDATION

Predation is a major cause of mortality in many

populations of primates [Isbell, 1994], and those wholose a relative in a predatory attack show clearevidence of stress. In a population of chacma baboonsthat suffered high levels of predation the physiolo-gical markers of stress diminished in the weeksfollowing a kill, as the bereaved individuals rein-forced social bonds with other group members[Cheney & Seyfarth, 2007]. Primates engage in avariety of anti-predator behaviors, several of which areobservable in and around sleeping sites [Anderson,1984, 1998]. If predators kill group members ata sleeping site, then that site may be abandoned[yellow baboons: Altmann & Altmann, 1970]. On theother hand, if individuals die in a less traumatic

manner at a sleeping site, abandonment may be lesslikely. A remarkable example of this was described inHanuman langurs [Mohnot, 1971]. Although mostmembers of a large (more than 80 members) troopdied at and around a habitual sleeping site, probablydue to drinking contaminated water, the survivingmembers continued to return to sleep at the site.They did so in spite of witnessing their dead group-mates and relatives decomposing and being sca-venged by crows and vultures, and the stench ofdecomposing corpses of the langurs and cattle whohad also died. Other authors have also commentedthat the foul odor of decomposing flesh does not

appear to deter mothers and others from transport-ing and manipulating corpses [Biro et al., 2010;Fashing et al., 2010; Warren & Williamson, 2004; butsee also Merz, 1978]. One might ask whetherprimates confronted with the odor of a non-

witnessed death upon arrival at a sleeping site mightbehave otherwise.Primates can also be predators. Sometimes this

includes killing and eating members of their ownspecies (as in cases of cannibalism of infants), butpredation by primates usually means killing andeating other species. Although prey are usually killedbefore consumption begins, baboons [Strum, 1987]and chimpanzees [Boesch & Boesch, 1989; Teleki,1973b] sometimes start consuming their victimbefore it is dead. Killing an animal before eating itis clearly advantageous as it removes any possibilityof the prey defending itself or escaping, so anypreference for starting to eat before it is fully dead

requires explanation. Chimpanzees clearly preferfreshly killed meat; they are much less interestedin consuming animals that are found already dead[Stanford, 1998].

Like other phenomena described above, primatecarnivory raises several questions about their aware-ness of death. At the very least they would appear tomake the distinction between the capacity for agency(alive) and the absence or cessation of agency (dead).This basic distinction emerges relatively early inhuman children, by around 4 years of age [Barrett &Behne, 2005], though other aspects of death aware-ness in children are not mastered until much later

[e.g., inevitability, causation in the form of breakdownof bodily functions; see Slaughter & Griffiths, 2007].

TOWARD A PRIMATE THANATOLOGY

The literature contains many descriptions ofhow nonhuman primates respond to the deaths offamily members, other members of their group,extra-group members, and other species. In manycases the consequences for feeding, ranging, socialdynamics, and demography have been considered,but with the exception of death-induced stress anddepression in survivors, the reports do little toelucidate primates awareness of death, its psycholo-

gical rather than its socioecological significance.Further careful and fuller descriptions of how deathimpacts on individuals behavior are required to helpbuild a picture of death awareness. Field researchersare best placed to inform on the multiple causes ofdeath and its effects on a wide range of behaviorsacross different stages of the lifespan, but there isalso a role for observations in captive primates. Oneearly description suggested possible attempts torouse a dead companion by a young chimpanzee[Brown, 1879], something that may occur in the wild[baboons: Altmann & Altmann, 1970; chimpanzees:Boesch & Boesch-Achermann, 2000]. Some attempts

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have even been made to communicate with signlanguage-trained apes about death [Fouts, 1997;Patterson & Gordon, 1993], but careful recordingof behaviors in response to naturally occurringdeaths seems likely to provide more valuable data.

Shortly before he died, an ailing captive male pottoreceived grooming from the other two members ofhis group [Cowgill, 1972], reminiscent of eventsobserved in a small group of chimpanzees [Andersonet al., 2010]. In both the pottos and chimpanzees, thesurviving individuals showed decreased appetitefollowing the death, although the pottos habit ofleaving enough food for another individual was notobserved in the chimpanzees (though no attempt wasmade to record this).

Bertrand [1969] briefly described the responsesof captive stumptailed and liontailed macaques to theintroduction of dead conspecifics. The monkeys werehighly interested in the corpses and showed puz-

zling behaviors including sniffing, extensive groom-ing which developed into pulling out chunks of fur,and one attempted mount of a dead female by a male.Corpses of familiar group-members were approachedand contacted quickly, whereas those of unfamiliarindividuals were treated more cautiously. Althoughnot a controlled experiment, Bertrands accountdraws attention to the possibility of experimentalinvestigations aimed at clarifying primates percep-tion of death. In one experiment the response offemale squirrel monkeys whose infants had died justshortly after birth or after two weeks were presentedwith their own dead infant or another dead infant.

The earlier the age of the infant at death, the lessdiscriminating the mother was when presented witha corpse [Kaplan, 1972]. Responses included vocali-zations and retrieval postures, and attempts to liftthe corpse, all of which decreased with increasingtime after the death of the infant. In an interestingdiscussion of animals mental representations ofdeath, Allen and Hauser [1991] describe experimentson the responses of social insects to dead conspecifics.They also explore how experimental approaches (forexample, using playback vocalizations of deadindividuals) might be useful for providing insightinto how nonhuman primates might conceive ofdeath in other individuals, while also recognizing

ethical issues that might be raised by experimentalresearch on this subject.

In conclusion, observations of how individualsrespond to death in both captive and wild settingscan be used to build a comparative picture of themeaning of death among primates. It is a topic thathas been largely neglected by primatologists, mostlikely due to the lack of preparedness to record theevent (especially in the field), and the conventionalpractise of removing (and sometimes euthanizing)very sick individuals in captive groups, or of swiftlyremoving a dead individual. However, the decision toallow an ailing, elderly chimpanzee to die naturally,

attended by her group gave the opportunity to gainnew insights into death awareness in chimpanzees[Anderson et al., 2010]. In particular, it was possibleto monitor the responses of survivors as theyremained in the vicinity of the corpse throughout

the night; under natural conditions survivors even-tually need to abandon the corpse in order to forage.Hopefully that report and other recent papers [Biroet al., 2010; Fashing et al., 2010] will encourageresearchers to give greater consideration to thepsychological consequences of death, leading to thepublication of more observations of this inevitableand momentous aspect of primates lives.

ACKNOWLEDGMENTS

All research reported in this manuscript adheredto the American Society of Primatologists Principlesfor the Ethical Treatment of Primates.

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Fashing P, Nguyen N, Barry T, Goodale C, Burke R, Jones S,Kerby J, Lee L, Nurmi N, Venkataraman V. 2010. Deathamong geladas (Theropithecus gelada): a broader perspec-tive on mummified infants and primate thanatology.

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