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Non-Human Animal Responses towards the Dead and Death:


A Comparative Approach to Understanding the Evolution of
Human Mortuary Practices
Alexander K. Piel and Fiona A. Stewart

responses seem maladaptive, e.g. consumption of bodies


INTRODUCTION
(Macbeth et  al. 2007). The type of death and relations
The awareness of mortality is a human universal, although between the dead and the survivor also play a role (Parkes
when and what factors contributed to its conception are 1985). Responses vary in intensity, duration, and whether
poorly understood.That is, what biological, ecological, or the process is immediate or delayed after the death.
cultural pressures encouraged its manifestation in Homo Additionally, there may be a learned component. That
sapiens? It is not until we examine the Palaeolithic that is, whilst children have strong feelings at a death – char-
archaeological techniques can be used to reveal human acterised particularly by aggression, anxiety, sadness, and
attention to, and perhaps understanding of death; in other fear caused by the separation inherent in death (Hutton &
species, no such material artefacts exist. Nonetheless, by Bradley 1994) – adults instead understand the complex-
examining extant animal responses to the dead we may ity of death, and more fundamentally, experience it as
learn of the emerging capacities to perceive death, and a stage in the life cycle (Slaughter 2005; Slaughter &
subsequent treatment of it within human and other ani- Lyons 2003).
mal societies. Despite there being a rich literature examining human
Humans exhibit diverse cultural variation in mortu- responses to death, we know little of how other ani-
ary practices (Huntington & Metcalf 1979), in which mals respond to dead companions. Understanding to
treatment of dead bodies ranges from their consump- what extent humans and other species exhibit similar
tion to the placement of them as far above (Martin 1996) responses to death may inform on how these traits have
or below ground as possible (Andrews and Bello 2006). evolved and to what extent responses to death may be
Some treatment patterns, however, are consistent with associated with our increased relative brain size and soci-
what we would predict given our species’ hyper-sociality ality. Non-human animals also exhibit wide variation
and environment (e.g. home-base use). For example, liv- in responses to death (see Table 2.1). These include any
ing in close societies means burial (or destruction) of change in behaviour following the death of a conspecific,
dead bodies is important for hygiene and thus fitness. and in particular treatment of the dead – any behaviour
Some responses to dead (or to the death of) compan- directed towards the carcass. Evidence from other species
ions are universal and also consistent with evolutionary is limited and anecdotal due to the difficulty of observing
explanations. For example, Littlefield & Rushton (1986) sick or wounded animals in the wild, which often retreat
showed that mothers grieve more intensely than fathers, from their social group shortly before death (Hart 1988).
and both grieve more intensely for dead men than dead In captivity, observations are also few as it is common
women. Healthy children are mourned more intensely practice to remove dying individuals from their social
than unhealthy children, and parents with fewer chil- group (Anderson et  al. 2010). Even when responses to
dren grieve more intensely than those with many chil- death might be observed, anecdotes make for weak anal-
dren. Evolutionary biology, however, seems unlikely to yses, thus discouraging researchers from publishing them.
explain the range in human responses to death, as other Published reports of negative results, e.g. animals that do

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Table 2.1. Species and observed responses to dead conspecifics

Common name Scientific name (s) EQ^ Social system Responses to carcass (observation frequency 0–3*) Reference(s)

Hygienic Investigative

Aggressive Sexual Supportive

Honeybee Apis mellifera <1.0 Eusocial 3 0 0 0 Spivak 1996


Ant Pogonomyrmex barbatus <1.0 Eusocial 3 0 0 0 Brown et al. 2006;Wilson 1971
Strumigenys lopotyle
Atta colombica
Aphid Pemphigus spyrothecae <1.0 Eusocial 3 0 0 0 Benton & Foster 1992
Sand martin Riparia riparia NA Cohesive 0 0 1 0 Dale 2001
Mallard Anas platyrhynchos NA Cohesive 0 0 1 0 Moeliker 2001
Ground squirrel 1.5–2 Cohesive 0 0 1 0 Dickerman 1960
Rat Rattus rattus 0.4 Solitary 3 0 0 0 Pinel et al. 1981
Mole rat Heterocephalus glaber 0.75–1.5 Eusocial 3 0 0 0 http://www.nytimes.com/2008/09/02/
science/02angi.html
Ringtail lemur Lemur catta <1.0 Cohesive 0 0 0 2 Nakamichi et al. 1996
Gelada baboon Theropithecus gelada 1.74 Cohesive 0 0 0 2 Fashing et al. 2010
African elephant Loxodonta africana 1.88 Fission fusion 0 2 2 2 Douglas-Hamilton & Douglas-Hamilton 1975;
Masson & McCarthy 1996; Moss 1988;
Wittemyer & Douglas Hamilton 2005
Chimpanzee Pan troglodytes 2.38 Fission fusion 0 2 2 2 Anderson et al. 2010; Anderson 2011; Biro
et al. 2010; Cronin et al. 2011; Hosaka 2000;
Stewart et al. 2011;
Bottlenose dolphin Tursiops aduncus 5.6 Fission fusion 0 2 2 2 Bearzi 2007; Dudzinski et al. 2003;
Humpback whale Megaptera novaeangliae 0.18 Fission fusion 0 0 1 0 Pack et al. 1998
Human Homo sapiens 6.28 Fission fusion 3 0 0 3 Huntington & Metcalf 1979
Notes: ^ EQ: Encephalisation quotient, ratio of actual brain mass to predicted brain mass for an animal of a given size;
* Responses to conspecific carcasses summarised as ‘Hygienic’ (removal/destruction of corpse to clean living area or reduce exposure to disease) or ‘Investigative’ (visual or physical attention to the corpse,
e.g. aggressive, sexual, or supportive. Supportive investigation may include carry, move, seeming to assist, clean or groom body). Observation frequency of such behaviours was rated from 0–3 (0 – no reports,
1 – a single anecdote reported, 2 – greater than one report, 3 – commonly reported).

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not respond to dead conspecifics, are even more rare. size and social structure may reveal important social or
Although this is not an exhaustive review, we have tried environmental factors in the evolution of human mor-
to include examples from a range of species, and also tuary practices.
negative observations where available. This paper is nec- Pettitt (2011) used a broad framework to understand
essarily biased towards those species where most descrip- the development of mortuary rituals in human evolu-
tions are available. We thus focus primarily on responses tion, ranging from behavioural evidence of extant pri-
to death in social species, and in particular the Primates, mates to archaeological signatures in prehistoric human
with an emphasis on chimpanzees (Pan troglodytes). societies. In his review of chimpanzee responses to death,
Historically, animal responses to death have been stud- he sought to model key behavioural patterns, suggest-
ied in the framework of trying to understand the men- ing that they form the blueprint of mortuary activity
tal and emotional states of other species. For example, within the Hominidae. A  primatological perspective
in a discussion of concept attribution in non-humans, on death may reveal whether or not other members of
Allen & Hauser (1991, 230) described baboon responses the Hominidae share with us ‘core’ activities in response
to death as ‘...like the distraught parents who will not to death. Classifying behavioural responses into realms
accept the fact of their child’s death’. Similarly, African of e.g. Communication, Social Theatre, and Morbidity,
elephant (Loxodonta africana) investigation of bones has Pettitt demonstrated how these common threads of
been described as ‘mourning’ (Masson & McCarthy response behaviour might unite hominoids and homi-
1996). (Later experimental work demonstrated that nins, suggesting their roots in the earliest members of the
whilst there appears to be a clear preference for bones Hominidae.
and tusks of conspecifics over those of other species, there Although disagreement and uncertainty persist over
is no evidence that individuals treat remains of kin dif- attributing thoughts and feelings to other species, espe-
ferently over non-kin: McComb et al. 2006). In addition cially in the context of death, greater documentation of
to potentially analogous emotions between humans and suggestive behaviours, especially across the Primate order,
other animals in their responses to death, both also share helps to strengthen and to test models that seek to explain
adaptive behaviours. For example, some species, including the roots of these behaviours. What Pettitt’s model lacks
humans, remove carcasses from their dwellings, ridding is a broader examination of death-responses across other
homes of otherwise potentially disease carrying agents species. Using such a cross-taxa comparative perspective
and possible targets of dangerous scavengers or predators. may identify those responses that are universal and adap-
Other social species thoroughly investigate carcasses, a tive, as well as others that may be unique to humans,
potentially maladaptive response (see Table 2.1). Without hominoids, or other large-brained, social species. This
comparative research into these responses across species, paper aims to explore the diversity of and influences on
we cannot explain their diversity. non-human animal responses to death. From a compila-
Furthermore, despite a surge of recently described tion of anecdotes, we describe whether such behaviour is
primate responses to death (Anderson 2011; Anderson supportive, aggressive, or sexual, and to what extent the
et  al. 2010; Biro et  al. 2010; Cronin et  al. 2011; Fashing relationship between the dead and survivors influences
et al. 2010; Stewart et al. 2011; Whilde & Marples 2011), subsequent responses. Specifically, we try to answer the
Anderson (2011, 3) concluded that these reports ‘do little question of whether any animal patterns exist that are
to elucidate [primates’] awareness of death, its psycho- associated with larger relative brain size (here measured
logical rather than its socioecological significance’. But as the encephalisation quotient – EQ: see Table 2.1) or
a better understanding of this ‘socioecological signifi- with sociality, such that the evolution of human responses
cance’ may implicate phylogeny, social system, physical to death can be reconstructed.
environment, or life history in explaining behavioural
responses. For example, from cetaceans to hominoids,
Innate Mechanisms
parallel behaviours exist, e.g. atypical vocalisations, tac-
tile investigation, grooming, and attempts to revive Several species respond to the death of conspecifics in
(Anderson et al. 2010; Cronin et al. 2011; Dudzinski et al. what can be clearly seen as adaptive behaviours. Wilson
2003). Given the presence of the same characteristics in (1971, 278–9) described ant responses to the death of
human burial ritual (Huntington & Metcalf 1979), com- conspecifics, including the carrying of corpses to ref-
parison of responses across taxa that vary in relative brain use piles (observed in Pogonomyrmex barbatus) and piling

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of corpses into rings around nest entrances on the for- necro-socio-sexuality common in the animal kingdom
est floor (observed in Strumigenys lopotyle; see similar in or are these isolated incidents of pathology?
social aphids: Pemphigus spyrothecae, Benton & Foster 1992; On review, socio-sexual behaviour with carcasses
and leaf-cutting ants:  Atta colombica, Brown et  al. 2006). appears in several species. In their observations of the
Aphids that carry out ‘housekeeping’ behaviours, includ- responses of three male humpback (Megaptera novaean-
ing removal of the dead, have reduced life spans, highlight- gliae) whales to the death of a rival, Pack et  al. (1998,
ing the benefit of these hygienic behaviours to the colony 869) described in detail a diverse behavioural repertoire,
(Benton & Foster 1992).Wilson (1971) carried out experi- ranging from examples of epimeleticy2 to dominance
ments to identify the mechanism triggering these behav- displays and copulation attempts. Immediately before the
iours, concluding that individuals ‘recognise corpses on the male died, all four individuals showed intense compet-
basis of a limited array of chemical breakdown products’. itive displays (which was the likely cause of the death),
Support for this hypothesis came shortly thereafter with but despite, or perhaps because of this, one of the males
the work of Pinel and colleagues (1981), who showed not stayed with the dead individual for over four hours after
only that rats (Rattus rattus) bury dead conspecifics, but the death. His visible penis and pulsating genital slit dur-
also that the behaviour is at least partly under the olfac- ing this period suggested an unusually high state of sex-
tory control of compounds released during decomposi- ual arousal. Bailey & Zuk (2009), in a comprehensive
tion, cadaverine and putrescine. The experiments revealed review of same-sex behaviour in animals, found no cases
that the instinct to bury is so strong that rats will bury in whales, suggesting that this behaviour was unique and
even individuals that are alive if they detect those poly- in response to the dead individual.
amines. Mole rats (Heterocephalus glaber) show a comparable Dudzinski et al. (2003) described the responses of dol-
behaviour, quickly detecting a corpse in their den, before phins (Tursiops aduncus) to conspecifics off Mikura Island,
dragging, kicking, or carrying it to the communal latrine. Japan. In one observation, six to eight dolphins spent
‘When the latrine is filled they seal it off with an earthen almost three hours with a male carcass, focusing almost
plug, presumably for hygienic reasons, and dig a new all their attention on its genital area. All male dolphins
one.’1 Honeybees (Apis mellifera) likely respond to simi- at the carcass site had penile erections, emitted vocalisa-
lar chemicals, removing parasite-infected or dead brood tions that differed from the normal repertoire, and spent
members (Spivak 1996), but they encase small mammals much time chasing other males away. In other contexts
that get stuck and die in their hives in resin collected from with living conspecifics, these behaviours are described
trees, perhaps because they are too small to move them as mate guarding. Even after surfacing to breathe, they
(G. Robinson, pers. comm.). Whilst these descriptions returned immediately and directly to the carcass. The
suggest behaviour that is explained most parsimoniously behaviours towards the carcass were both aggressive
by the removal of disease-carrying agents from enclosed (head-scanning), and affiliative (sexual), as if individuals
dwelling-spaces (and are noted as hygienic behaviours in were unsure how to behave. In another two-day observa-
Table 2.1), they also elucidate one of the biological mecha- tion of responses to a dead female, male dolphins showed
nisms for how animals detect a dead individual. no sexual arousal but were aggressive to researchers who
tried to retrieve the corpse. The male dolphins ‘assumed
aggressive actions (S-postures, jaw clasps) at swimmers.
Necro-Socio-Sexuality
The males then nudged and pushed at the carcass with
Not all responses, however, suggest this recognition. their rostra, pectoral fins and bodies, and swam belly-to-
Dickerman (1960, 404), in an opportunistic observa- belly to carcass...’ (Dudzinski et  al. 2003, 187). These
tion of a dead female ground squirrel, watched a male descriptions reveal increased arousal levels, and possible
approach and lay down beside her in a copulatory confusion at the lack of response, and overall state of the
posture:  ‘...undoubtedly, the flexed “female position” dead individual.They also reveal an unusual combination
of the dead animal released the copulatory drive in the of behaviours not seen together in other contexts.
male.’ The same mechanism may be invoked to explain
Moeliker’s (2001) description of male homosexual nec-
Relationship Quality
rophilia in mallard ducks (Anas platyrhynchos).Whilst both
homosexual and necrophilic behaviour have been seen in One relevant factor in variation in responses to death
mallards, no one before had seen them simultaneously. Is may be the relationship between the dead individual and

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the surviving group members. Given the importance of all the individuals involved (infant, mother, male) were
relationships to social animals, from alliance formation in predictive of how males treat dead infants.
dominance take-overs to cooperative foraging strategies, Examples of responses to dead chimpanzee infants
we hypothesise that relationship quality also influences date from almost a half-century ago, from the earliest
how individuals respond to dead conspecifics. We thus studies at Gombe, Tanzania. These reports often centred
predict that individuals that are more closely affiliated on post-mortem cannibalism of infants (Bygott 1972;
with the dead will exhibit stronger reactions, either in Goodall 1977). In her extensive review of infant killing at
immediate or longer-term behavioural changes. Gombe, Goodall (1977) detailed infant handling and kill-
ing, as well as treatment of the body. Both Goodall (1977)
Dead Infants and Bygott (1972) reported sniffing, poking, touching,
Most observations of animal response to death across examining, and grooming of the body, plus more aggres-
taxa, especially in primates, describe behaviours between sive patterns, including the corpse’s incorporation into
mothers and infants (although see Bearzi 2007:  Tursiops male charging displays. In most cases, carcasses were car-
aduncus). Nakamichi et al.’s (1996) report of seven (infant) ried around for amounts of time varying from hours to
deaths of L.  catta in Berenty Reserve, Madagascar days but then were abandoned.
included descriptions of visual and vocal behaviour Boesch & Boesch-Achermann (2000) detailed the
that showed extended interest in the carcass for several responses of Tai chimpanzees in Ivory Coast to the death
hours post-mortem by mothers, especially in their ret- of a two year-old male, Bambou. In response to Bambou’s
icence to leave dead infants. Unrelated group members death (probably the result of a broken neck), his mother
sniffed, touched, or licked the carcasses, whilst six of the made loud alarm calls and carried the body for almost
seven mothers beginning to travel moved back and forth two days. There was much interest in Bambou’s body
between the group and the dead infant before eventually by community members, but no aggression was exhib-
leaving it behind. None of the mothers carried their dead ited. Instead, individuals smelled the carcass, emitted soft
infants, however. ‘hoo’ calls (usually emitted in contexts of puzzlement and
Mothers’ responses to infant deaths have also been distress – Goodall 1986) and left silently after almost four
studied experimentally. Five squirrel monkey (Samiri sci- hours. Shortly after departing, however, Bambou’s mother
ureus) mothers whose infants died were presented with returned to collect her dead son’s body. She carried him
the carcasses of their infants and those of other females. for 20 metres, before leaving the carcass behind.The alpha
For all mothers, the age at which an infant died was most male guarded her (and the carcass), periodically during
predictive of her responses (that is, the older an infant this period, at the same time displaying at her.
was at death, the more often the mother discriminated More recently, Biro and colleagues (2010) described
her infant from another’s offspring; Kaplan, 1973). This the carrying of dead infants in the Bossou community,
example suggests, at minimum, that familiarity increased Guinea, where individuals of all age-sex classes ‘attempted
maternal response to the death of an infant; however, to touch, poke, or handle the bodies’ carried by their
older offspring have also received greater investment mothers for up to 68 days after the infant’s death. In con-
than younger ones. Kaplan’s observations could there- trast to other observations from captivity (Matsuzawa
fore also indicate that a difference in maternal invest- 1997) and the wild (see below), no aggression was ever
ment influences a mother’s response to the death of an observed towards the carcasses. A  recent report from
infant. Chimfunshi Wildlife Orphanage Trust, Zambia represents
Infant relationships with other group members may one of the first descriptions that systematically quantifies
also influence post-mortem behaviour. Merz (1978) a mother’s response to her dead infant. Cronin and col-
recorded the behaviour of male Macaca sylvanus to dead leagues (2011) recognised there is a paucity of evidence
infants in a semi- free-ranging population living in La that examines how, in this transitional process, a mother
Montagne des Singes, France. Males extensively handled distances herself from the infant carcass. Measuring the
the carcasses, roughly swinging, nibbling, and tugging at proximity and interaction between mother and dead
them. Merz (1978, 753) found that those males that had infant across time, the authors suggested that their obser-
engaged with an infant in life continued to do so after vations specifically inform on how chimpanzees respond
the infant died, giving evidence of a ‘lasting personal rela- to the ‘premature severing’ of the mother–infant bond,
tionship’. She concluded that the relationships between slowly accepting the change in state of their offspring.

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Finally, Fashing et al. (2010) detailed the responses of agitation and investigation with the trunk and feet, are
wild gelada monkeys (Theropithecus gelada) to dead infants, well known (Douglas-Hamilton & Douglas-Hamilton
where carcasses evoke considerable interest from female 1975; Moss 1988). In their observations of five unre-
group mates in particular. Females carried their own lated families (all matriarch herds) visiting the carcass of
dead infants for approximately 1–4 days before abandon- a recently dead matriarch in Samburu National Reserve,
ing the body, but exhibited limited or no interest in the Kenya, Douglas-Hamilton and colleagues (2006) sug-
death of adult or juvenile conspecifics. The authors also gested a ‘generalized response’ from conspecifics, includ-
described the death of a mother-infant pair whose weak- ing kin and non-kin. Like primates (described below),
ness eventually prevented them from keeping up with the closest associate of the dead individual spent the most
troop. On the first day the pair failed to follow the troop, time in proximity to the carcass, for up to five days after
group members looked back often in the direction of the death.
the pair, but eventually moved on to forage. Even upon Merte et al. (2008) described the reactions of 30 ele-
return to the sleeping site where they had all slept the phants to a freshly-dead male herd member, and how
night before, no evidence was observed of any attempt behaviours such as sitting on or mounting the carcass were
to locate the weakened mother-infant pair. The mother shown that ‘sought a response’ from the elephant carcass.
died first, infant at her side; the infant died alone the Sex differences were dramatic, with males comprising
following day. 97% of nearest-neighbour data over the first 2.5 hours
Evolutionary biology explains well the extensive after the death, despite a matriarch-led group watching
interest mothers exhibit in dead offspring. Mammals that nearby. Three males in particular – thought to be close
experience long gestation and development will benefit associates – monopolised the carcass, performing almost
with the successful survival (and subsequent reproduc- 85% of all behaviours seen. Associations during life may
tion) of their offspring thus premature abandonment of sufficiently explain sex differences in these ‘concerned’
a suffering, but viable offspring has tremendous fitness (Douglas-Hamilton et  al. 2006, 100)  behaviours:  given
costs. Silk (1999) also reminds us that infants are inher- that males and females each form same-sex bachelor and
ently interesting, and at least for living infants, should nursing sub-groups (Wittemyer & Douglas-Hamilton
be even more attractive to females. However, a consis- 2005), this sex difference in how carcasses are treated
tent female sex-bias is absent in observations of dead may reflect association during life, rather than curiosity
infant-interactions in primates. Rather, from the above at death.
reports, male primates may exhibit more interest than Summarising chimpanzee responses from Mahale
females, and use the carcasses as a tool in intrasexual Mountains National Park, Tanzania, Hosaka et al. (2000)
encounters (Merz 1978). Finally, those individuals that discussed the diversity of ways that chimpanzees respond
spent time with the infant during its life continue to to the death of community members (excluding those
interact with it after its death, indicating the importance caused by inter-community aggression). They suggested
of relationship quality in predicting post-death responses. that level of decomposition and cause of death influ-
ence emotional state, ranging from fear to curiosity, with
Dead Adults females and juveniles tending towards the former and
There are fewer documented cases of behavioural males the latter. Those feelings are expressed through
responses to dead adults than to youngsters. In primates, vocalisations, which are usually emitted as warnings in
the responses of dependant offspring to dead mothers response to a threat (e.g. wraa barks) or when curious or
are the most commonly observed and offspring tend to (e.g. hoo calls). As with the macaques described above,
remain close to their mother’s body (e.g. Stewart et  al. Mahale males are often aggressive with conspecific car-
2011; Fashing et al. 2010; Goodall 1986), and sometimes casses, using them in charging displays. Chimpanzees also
die shortly thereafter (e.g. Fashing et al. 2010). In chim- show similar behaviour to the carcasses of other animals,
panzees, offspring may be adopted by other members of whilst other primates pay little attention to them (e.g.
the community allowing them to survive to adulthood Cercopithecus aethiops: Struhsaker 1967).
(although see below; Goodall 1986). Teleki’s (1973) observations from Gombe and Stewart
In elephants, there is general interest in sick, dying, et  al.’s (2011) from the same community 40  years later
or dead individuals, and behaviours upon encounter- are rare detailed descriptions of chimpanzee responses to
ing bones of conspecifics, in which they exhibit intense the death of an adult group member. Teleki described

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reactions to the sudden and dramatic death of an adult compassion and empathy (see also Anderson et al. 2010).
male community member, Rix, who fell from a tree and Unfortunately, as with the Gombe examples above, the
broke his neck. Behavioural responses varied across indi- authors did not describe the pre-death relationships
viduals, and were hypothesised to be influenced by age between the dead (Tina) and those who interacted with
or social relationship. Some companions stayed with the the body: thus further analyses of the role of relationships
corpse for many hours, and almost all made ‘wraa’ barks, cannot be made.
prompting Teleki to conclude that such vocalisations may In summary, in elephants and chimpanzees, both kin
have a special significance in the context of a dead com- and non-kin express an interest in dead companions,
munity member. although in both taxa, association during life appears to
Stewart et al. (2011) made similar observations of the explain greater interest after death. In chimpanzees, espe-
responses of 18 individuals to the death (following a long cially, males express more interest than females, although
illness) of an adult immigrant female, Malaika. Initially, given male philopatry and dominance over females,
the corpse was visited by a succession of individuals males are both more likely to be related and able to sup-
who one-by-one briefly investigated the body, whilst press female access.
other individuals watched from above. Soon thereafter,
eight individuals formed a silent, tight circle around the
Environmental Explanations
body, mostly looking, but a few sniffing or grooming the
body. During the observation, individual young males Whilst reports from chimpanzees routinely explore the
sequentially monopolised Malaika’s body, in turn displac- role cognition may play in responses to death, Fashing
ing younger chimpanzees (including Mambo, Malaika’s et al. (2010), in comparing extensive dead infant-carrying
four-year old offspring who spent the most time in prox- in baboons and chimpanzees, suggested instead that the
imity to the body). The young males’ persistent manip- physical environment requires more attention. They
ulation of the carcass suggested they may have been argued that perhaps cold or dry climates delay decom-
frustrated with her lack of response, or else were using position, and thus promote more interest from group
her body as a tool in displaying to community members. members. Additionally, that wild animals need to travel
Malaika’s body was not left alone during the observa- and forage may preclude the more complex behaviours
tion and was eventually dragged for over 60m by at least observed in captivity (Anderson et  al. 2010). However,
four individuals. This dragging sometimes seemed to be appropriate climatic conditions, or time afforded by cap-
attempts to monopolise access, as individuals dragged the tivity, although permitting ‘extensive interest’, do not
body away from others, whilst at other times, seemed to explain it. For example, in describing a lack of interest by
be attempts to haul the corpse with the party after other community members (excluding the mother) in a dead
individuals had begun to travel. In total, her companions chimpanzee infant in Kibale National Park, Uganda,
spent at least four hours with the carcass before abandon- Wrangham3 argued that even ‘the capacities of empathy
ing it to begin to travel. As with Teleki’s interpretations, and cooperation that captive experiments show chim-
the authors found a relationship between age and sex panzees to be capable of must sometimes fall victim to
class and interaction with the carcass, with younger males baser urges due to the harsher life of a wild chimpanzee
exhibiting more aggression than females and elder males. in a forest’. However, these observations contrast with
Finally, at Tai, Boesch & Boesch-Achermann (2000) the above observations from Gombe and Tai of exten-
recounted community responses to the sudden death sive interest expressed for prolonged periods of time by
(possibly from a leopard attack) of a 10-year old female, chimpanzee community members to both infant and
Tina. The community showed a suite of behaviours in adult carcasses.
response to her death, from beating and dragging of the
body to sitting around the carcass in silence. The authors
Death Versus Dead
reported sex differences, with males spending more
time with the carcass than females, and one male spent The above reports provide a glimpse into how animals
almost five hours with it. Blood was regularly licked respond to a dead adult conspecific, but not to death
from the wounds of living individuals, but none was itself. Across human societies people grieve the loss of
licked from Tina. From their observations, the authors companions on their death. This process is a response
raised the possibility that chimpanzees, like humans, have to the permanent absence of the individual (e.g. death),

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versus examples above, of responses to a dead body. We it remains unknown if the death site is also avoided in
could find only three examples of the former, two from the wild. The contrast in behaviour pre-, during-, and
captive primates, which provide evocative evidence of post-death seen in Anderson et al.’s study encouraged the
human-like grieving. In 1961, the death (and removal) authors to draw conclusions about the possible mental
of a male potto (Perodicticus potto) in a Yale University and emotional state of the surviving chimpanzees, specif-
Laboratory gave researchers an opportunity to monitor ically whether empathy and self-awareness – traits shared
the responses of his remaining two cage-mates, a male and by humans and chimpanzees – allow us also to share with
a female, to permanent absence (Cowgill 1972). After the them an awareness of mortality.
male’s death, the two surviving pottos did not consume
all the food provisioned to them but rather appeared to
Mal-Adaptive Investigation?
leave enough food each day for another animal. When
Cowgill decreased food portions, thereby controlling for Removing or isolating a carcass from one’s home base
the possibility that the pottos were simply satiated, they makes adaptive sense by thereby reducing potential
continued to leave food even after food portions were exposure to disease. Elephants, dolphins, and chimpan-
cut to half of their initial amounts, to the point that she zees, however, spend significant time investigating dead
feared the surviving pottos would starve! bodies. Compared to the responses of ants, honeybees,
In the only case from the wild, Goodall (1986) and mole rats, all which live in confined spaces that may
described an almost fully independent juvenile ‘Flint’ facilitate rapid pathogen transmission, such extensive tac-
showing symptoms of human like grieving: he remained tile interest in a dead body by nomadic organisms seems
with the body of his dead mother long after her death mal-adaptive. During this stage, behaviours associated
before himself succumbing to illness. Whether his symp- with high arousal, such as sex and aggression, are com-
toms of lethargy, lack of appetite, and his subsequent mon, presumably to gather more information about the
death were a result of illness or ‘grieving’ is unknown. unusual unresponsiveness of the carcass. These highly
Finally, Anderson and colleagues (2010) reported on investigative species share two other key features: (1) large
the death of an adult chimpanzee at Blair Drummond encephalisation quotients, and (2)  fission-fusion social
Safari Park, Scotland. Unique to this report were the systems (see Table 2.1). Fission-fusion social systems are
detailed video records made before, during, and after fluid and flexible, whereby individuals form temporary
the death. The authors described behaviours analogous sub-groupings that vary across space and time. Just as
to those that humans exhibit: chimpanzees appeared to fission-fusion systems have been argued to promote intel-
care for the individual before death, to test for signs of ligence, as well as theory of mind and self-conception in
life at the point of death, and to show signs of frustration hominoids (Potts 2004), so might it, combined with large
after death, as well as subsequently to avoid the place brains, have resulted in the ability to learn about death.
where the death occurred (after the body was removed).
They proposed that their observations differ in impor-
Knowledge of Death
tant ways from previous accounts:  first, whilst reports
from Gombe (Stewart et  al. 2011; Teleki 1973) and Tai Evidence from human infants suggests that they exhibit
(Boesch & Boesch-Achermann 2000) described excited empathetic behaviour from nine months, but cannot fully
and aggressive behaviours by conspecifics towards car- conceptualise death until six to nine years of age. Until
casses, Anderson and colleagues observed subdued, calm then, most children insist death is temporary, or revers-
behaviours, ‘strikingly reminiscent of human responses ible, associating it with sleep. Their initial responses to
to peaceful death’ (2010, R350). Also, at both Tai and death include increased aggression towards peers, a desire
Gombe, chimpanzees showed notable interest in the car- to know who was responsible, and concrete questions
cass and the place of death, even dragging the body as surrounding how the dead will eat and breathe (Hutton
much as 60m at Gombe. The opposite response was seen & Bradley 1994). Children struggle to verbalise how they
in Scotland, where individuals avoided the place of death feel about death, and often are obsessed with what the
for five consecutive days, despite having slept there the body looks like (Saunders & Kastenbaum 1997).
29 previous nights. However, studies of wild chimpanzees Many human cultures channel emotive responses
responses to death have not yet investigated home-range through religious and philosophical systems, ritual prac-
use pre- and post- death of a community member, so tices, and particular elements of social organisation to

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facilitate the acceptance and experience of death (Grof & know if non-human primates query those responsible
Halifax 1977). In non-human societies, such avenues for death, or how the dead will subsist, as human chil-
are unknown. However, given well-established cultural dren do. However, across populations, especially in wild
diversity in many behaviours in other species (especially chimpanzees and dolphins, survivors share some overt
chimpanzees – McGrew 2004, and dolphins – Krutzen tendencies, namely a propensity towards aggression, as
et al. 2005), it is possible that non-humans also have cul- well as vocalisations associated with stress and anxiety. In
tural activities related to death and dying. humans, weeping may represent incorporation of new
How do these behaviours compare across species? Rat information, including ‘a shift in denial...to assimila-
burial and insect embalming suggest that death-response tion of the actuality of the event’ (Marrone 1999, 514).
behaviours are triggered innately by the release of poly- The pattern described in Table 2.1 suggests that species
amines during decomposition, and need not be influ- of fission-fusion social systems and higher EQs exhibit
enced by social relationship or context. The adaptive more intense and possibly emotive responses to death;
value is clear – isolating decomposing carcasses reduces perhaps this is the same ‘assimilation of the event’ that
exposure to potential disease or scavenging predators. Marrone describes occurring in other species.
An increase in mortuary activity in humans could be
explained by the need for increased hygienic behaviours
Adaptive Denial of Death
as a result of a more fixed home base. The widespread
observations in cetaceans of sexual behaviour combined Pettitt’s (2011) interpretation of Tai chimpanzees’
with aggression, suggests heightened, if misdirected, responses to Tina’s death, which include unusual vocali-
arousal levels. That is, a carcass is neither a potential sations, sitting silently, grooming, displaying, and dragging
mate nor threat, yet it is simultaneously treated as both, her body, is that an unusual combination of behaviours
which mirrors chimpanzees and elephants in combining are exhibited which do not occur together in other con-
behaviours otherwise not observed in a single context. texts. Similar phenomena occurred at Gombe, Mahale,
Alternatively, lacking limbs to investigate a carcass, ceta- and Chimfunshi. Teleki (1973) suggested that the behav-
ceans may use sexual behaviour to learn about the state iour of certain individuals ‘...seemed to indicate aware-
of a motionless conspecific. ness of a change from activity to inactivity of a group
Stewart et al. (2011) discussed exploratory learning as member, but it remained uncertain whether any partici-
a possible explanation for the age-graded responses at pant grasped the conceptual difference between life and
Gombe, where juveniles and younger individuals (spe- death’, whilst Pettitt (2011, 37) concluded that ‘chimpan-
cifically males) showed more interest in a carcass than zees appear to be aware that death has occurred’. On
did older individuals. Cronin et  al. (2011) invoked a what level, then, do we expect chimpanzees (or other
similar explanation for observations from Chimfunshi, social and intelligent species) to be aware of death?
suggesting that mothers were gathering information Fear of death has been argued to be a human univer-
about response-levels of infants and so were learning sal (Becker 1973), and across societies ‘death anxiety’ is
about dying: described as the complex and amorphous set of feelings
aroused by thinking about death (Moore & Williamson
The behaviours expressed by the mother are consistent with the
suggestion that the mother was actively gathering this novel sen- 2003; Schultz 1979). Full self-awareness and a theory of
sory information about the dead infant. Conceivably, this infor- mind that allow for inter-subjectivity probably have been
mation could be remembered the next time she encountered propagated by positive natural selection and in some way
the same set of cues, and the implications of death  – that the benefitted ancestral hominins (Hauser 2009). Others have
individual is removed from one’s social environment – could the- argued to the contrary, that these same traits may actually
oretically be learned by chimpanzees.
be evolutionarily detrimental to an individual or species.
(Cronin et al. 2011, 420)
Specifically, Varki (2009) proposed that these traits bring
The question of whether mothers themselves learn about with them an awareness of death and mortality which,
death or the implications of it could be addressed by future ‘...far from being useful, the resulting overwhelming
studies on comparing responses to death in mothers who fear would be a dead-end evolutionary barrier, curbing
have or have not previously experienced infant death. activities and cognitive functions necessary for survival
Parallels between the responses of chimpanzees and and reproductive fitness’. Varki (2009) suggested instead
human youngsters to the dead are striking. We cannot that other hominoids’ (as well as cetaceans, elephants,

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Table 2.2. Behaviours seen in wild chimpanzees, dolphins, and elephants in response to dead conspecifics, under
the realms of ‘communication’, ‘social theatre’, and ‘morbidity’

Chimpanzees Dolphins Elephants

Communication
Unusual calls X X X
Gathering, loud calls X X X
Sitting in silence X X
Play & laughter X
Social Theatre
Aggressive displays X X X
Banishing of low-ranking individuals X
Males stay longer at corpse X X X
Morbidity
Dragging of corpse X
Smelling and investigation of corpse, including sexual X X X
Grooming of corpse X X
Modified from Pettitt 2011, fig. 2.2; X indicates presence of the behaviours in each species

and some birds) conception of death might have been early members of our genus and perhaps those of
blocked at some point during their evolution. According Australopithecus as well may have had the ability to learn
to Varki, a human-like awareness of death would inhibit about death in much the same way extant apes do.
otherwise positively selected behaviours. Following this, Consequently, these early hominins may have experi-
one might predict no human-like responses to the dead enced an emerging concept of death, demonstrated only
in other animals. How, then, do we explain similar behav- ephemerally, especially in their response to dead conspe-
iours between, for example, chimpanzees and humans? cifics. Exactly what that concept was, and how it mani-
Pettitt (2011) has argued that observations of other fested itself, we do not know, and may never. Despite
primates can help us identify core behaviours towards these uncertainties, the behaviours of extant apes (and
the dead that may reflect our shared evolutionary his- other species) that share with humans features of anat-
tory. He described these behaviours as falling into three omy and sociality, provide us insight into non-human
overlapping realms:  Communication, Social Theatre, animal treatment of the dead, and perhaps perception, of
and Morbidity. Behaviours associated with any of these death. Simultaneously, these behaviours offer a context
realms could reflect a focus on the individual, the carcass, from which we can examine the first material artefacts of
or the group. The reports from chimpanzees at Gombe, death-recognition in the archaeological record.
Tai, and Scotland contain features from all of these realms In this paper, we have argued here that fission fusion
(see Table 2.2), supporting Pettitt’s claim that embedded and large brains may play a role in predicting animal
within our primate ancestry lies the foundation for con- responses to dead conspecifics. We have outlined the
temporary human mortuary practices. diversity of animal responses, from insects to mammals.
However, we have found that these behaviours also With colony-dwelling insects, humans share the hygienic
occur in other fission-fusion, large-brained species, e.g. benefit of corpse-removal from a fixed home base. With
elephants and dolphins, and so these complex responses to chimpanzees, dolphins, and elephants, humans share
death instead may reflect a convergent path where, together a fission-fusion social system and hyper-investigative,
with inter-subjectivity and self-awareness, may come the potentially mal-adaptive behaviours towards carcasses.
ability to learn about death. Pettitt’s model may still apply, Fission-fusion systems require individuals to constantly
albeit expanded to species outside the hominoids. renegotiate relationships; intense investigation may result
from an ability to detect any changes in state and status
upon each reunion. To further differentiate the indepen-
CONCLUSIONS
dent influence of each of these factors, additional data
Human perception and treatment of death in the later are needed from small brained, fission-fusion species (e.g.
Palaeolithic are best understood through the lens of Crocuta crocuta) and large-brained, non fission-fusion spe-
archaeology. However, prior to the later Palaeolithic, cies (e.g. Gorilla gorilla). Regardless of the ultimate factors

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