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

Death among primates: a critical review of non‐human primate interactions towards their dead and dying. André Gonçalves, Susana Carvalho. Biological Reviews, April 4 2019. https://doi.org/10.1111/brv.12512

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


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III. PRIMATE THANATOLOGY:CONTEMPORARY REPORTS 

(1) Dead infants
 Females of several primate species have been observedpersistently to carry their deceased infants (sometimesfor prolonged periods of 10 days or more), regardlessof the circumstances that caused the fatality (Fig. 2). Otherrecorded behaviours include grooming, swatting flies awayfrom the corpse and sometimes even consuming part of it.Primatologists have described their expressions as ‘puzzled’,‘confused’ or ‘dazed’, which raises the question as to whetherthey have some, if any, understanding of death.These behaviours are striking because they seemmaladaptive. Whilst live infants are energetically costlyto the mothers who carry them, ultimately they increasereproductive fitness – something a dead immature offspringcannot do. Holding a lifeless corpse hinders locomotion,negatively impacting foraging and predator avoidance. Somewill solve these difficulties by adopting a tripedal gait, carryingthe corpse ventrally, using the neck and shoulder to wedgeit, drag it along the ground, or even carry it dorsally usingthe tail as an extra limb. While some hypotheses have beenproposed to explain post-mortem carrying (Table 1), it isstill a matter of debate which one offers the most powerfulexplanation. Because some are mutually non-exclusive it islikely that many factors, depending on context, contribute tothese behaviours (see Watson & Matsuzawa, 2018).








 
(a)Mother – infant dynamics
 Dead-infant carrying is the most prevalent thanatologicalbehaviour distributed in several primate taxa (Fig. 3). Thisshould not be surprising since: (i) primates follow a typicaltrend observed in many vertebrate species of high infantmortality (Bronikowskiet al., 2011); and (ii) unlike adolescentsand adults who are abandoned at their site of death, deadinfants and juveniles are usually carried by the mother forlonger durations, allowing easier detection. Nevertheless, themother will, invariably, cease to carry the corpse, leavingit unattended for progressively longer periods until finallyabandoning it (Jay, 1962; Nash, 1974; Green, 1975; Altmann,1980; Hosakaet al., 2000; Croninet al., 2011).Many authors have claimed that the mother ceases totreat her infant as a live one during this period – carryingit in awkward positions, by the leg or tail, upside down,using the mouth or dragging the corpse along the ground(van Lawick-Goodall, 1968; Green, 1975; Altmann, 1980;Luet al., 2007; Perry & Manson, 2009; Biroet al., 2010;Fashinget al., 2011). Green (1975), who conducted acomprehensive vocal study with wild Japanese macaques(Macaca fuscata), noted that mothers gave out particularvocalisations when their infants died, repeated whilst carryingthe infant or distant from it. Some have proposed thatinfantile colouration may elicitpost-mortemcarrying (Jay,1962; Alley, 1980; Rajpurohit, 1997), but this does notexplain why such behaviour occurs in females from myriad
primate species – some with flamboyant natal coats andothers non-conspicuous.Perry & Manson (2009) describe a case of a capuchinfemale (Cebus capucinus) carrying her stillborn, arguing thatshe behaved in ways which suggested an awareness ofher infant’s death, such as letting the infant be fullysubmerged in water. Although this could represent causalattribution, it may equally be a failure of perspectivetaking. Inexperienced Japanese macaque mothers havebeen observed to inadvertently drown their infants whendiving into the hot springs of Jigokudani Park for food (deWaal, 1996) and similar occurrences have been reportedamong baboons (Cheney & Seyfarth, 2007). Moreover,filial cannibalism duringpost-mortemcarrying has also beenwitnessed, suggesting that corpses may be re-categorisedas food (Altmann, 1980; Hsiang-Jen & Hsiu-Hui, 2008;Dellatore, Waitt & Foitova, 2009; Watsonet al., 2015; Tianet al., 2016; Tokuyamaet al., 2017; De Marco, Cozzolino &Thierry, 2018; Watson & Matsuzawa, 2018).Croninet al.(2011) propose that whilst displayingapproach – withdrawal behaviour towards the infant, themother is actively gathering novel death cues that she couldconceivably recall in equal situations (i.e. death of anotherconspecific). However, if the purpose of such knowledge isto prevent costly behaviours, findings from Sugiyamaet al.(2009) that there is no significant difference in carryingduration between younger and older mothers suggests that,at least in Japanese macaques, no such learning component was found. Moreover, reports on chimpanzees from Bossouillustrate that there may be an individual component. Of thefive infants that died during a flu epidemic, only two werecarried for extended periods (Biro, 2011). Jire transportedboth her dead infants: Jokro in 1992 and again Jimatoin 2003 (Matsuzawa, 1997; Biroet al., 2010). Similarly,in semi-ranging Japanese macaques, the same female wasreported carrying her dead infant for extended periods in2011 and again in 2013 (Watsonet al., 2015), although otherfactors such as cause of death could impact these responses(see Section III.1e).

(b)Group – infant dynamics 
The behaviour of group members who were not emotionallyinvolved with the infant is also of interest. Cheney & Seyfarth(2007) note that wild chacma baboons (Papio h. ursinus)donot attempt to handle dead infants and rarely grunt atthem as they would live infants. Similarly, Rajpurohit (1997)mentions that in Hanuman langurs, other members showlittle interest in dead infants – a finding also reported inother species (van Lawick-Goodall, 1968; Green, 1975;Luet al., 2007; Guoet al., 2016; De Marcoet al., 2018).Conversely, infants and juveniles express more interest inthe corpse (van Lawick-Goodall, 1968; Ciani, 1984; Croninet al., 2011; Liet al., 2012), some even playing with it (vanLawick-Goodall, 1971; Hosakaet al., 2000; Biro, 2011).Furthermore, juvenile and nulliparous adult females havebeen witnessed carrying dead infants relinquished by theirmothers (Warren & Williamson, 2004; Fashinget al., 2011).The mother occasionally restricts attempts by other groupmembers to access the corpse (Altmann, 1980; Gupta,2000; Liet al., 2012; Tokuyamaet al., 2017) (Fig. 4), withsiblings having broader admittance (van Lawick-Goodall,1971; Kano, 1992; Mulleret al., 1995; Matsuzawa, 1997). It is conceivable that such playful interactions may prepareyounger individuals for death recognition.The matter of stench avoidance is divisive. Byrne (2016)recounts a case in western lowland gorillas where the groupmembers, after initial interest, seemed to avoid and shunthe carrying mother after the body started to smell. BothGreen (1975) and Sugiyamaet al.(2009) report that Japanesemacaque group members actively avoided the mother of adead infant, presumably because of the putrid smell from thecorpse. However, among chimpanzees (Biroet al., 2010) andGelada baboons (Theropithecus gelada) (Fashinget al., 2011),no such avoidance is reported. That most mothers abandonthe infant within a week of death is also informative sinceduring this period the cadaver goes from bloating to activedecay – the stage of decomposition that emanates the moststench.Infant corpses are sometimes central to or incorporatedin the displays of male chimpanzees (Bygott, 1972;Matsuzawa, 1997). Adult males have also been known tocarry dead infants; most notably in semi-ranging Barbarymacaques (Macaca sylvanus) whilst interacting with othermales where the corpse is used for agonistic bufferingpurposes (Merz, 1978). In conjunction with other reports,Merz (1978) notes that handling was much rougher andof shorter duration than with live infants. Rare cases haveinvolved high-ranking individuals unsuccessfully adoptinglive orphans and continuing to carry them after death (Tayloret al., 1978; Notman & Munn, 2003). 

(c)Old World – New World dichotomy 
To the best of our knowledge, there are 13 publishedcases of dead-infant carrying among New World monkeys,comprising cebids, and atelids (see online Supportinginformation, Appendix S1). The lack of information on thisbehaviour may be partly due to the smaller numberof publications on New World primates. Anderson (2011)argues that their tropical habitats accelerate the decay ofcorpses and consequently their abandonment. Additionally,while Old World monkeys can be either arboreal, terrestrialor both, New World monkeys are almost exclusively arboreal(Fernandez-Duque, Di Fiore & Huck, 2012). Referring toan arboreal Old World species, the red colobus (Piliocolobustephrosceles), Struhsaker (2010) pointed out the difficulty ofcarrying a dead infant while leaping between trees – aclaim supported by other colobine cases (Colobus guereza:Onderdonk, 2000;Colobus vellerosus: Teichroeb & Sicotte,2008) and the observation that species that carry their deadfor long periods, such as snub-nosed monkeys (Rhinopithecusbieti) tend to be more terrestrial (Long & Kirkpatrick, 1994).Observer bias may also be involved; when reviewing theliterature on post-mortem carrying, the best-representedspecies were semi or fully terrestrial and inhabited accessibleareas or were in close proximity to human communities(Rajpurohit, 1997; Sugiyamaet al., 2009; Fashinget al.,2011). The only case of dead-infant carrying recordedamong prosimians comes from ring-tailed lemurs (Lemur catta)(Nakamichiet al., 1996), the most terrestrial lemur (Schmidt,2011). 

(d)Non-carriers 
Not all primates engage in corpse carrying althoughthere is evidence that they do show behavioural responsesto dead or dying infants (see Appendix S2). Strepsirrhinesand callitrichines generally do not carry dead infants, despitesome unsuccessful attempts at carrying having been reported.Nakamichi, Koyama & Jolly (1996) observed seven cases ofring-tailed lemur behaviour towards dead/dying infants.One individual carried her dying infant tripedally for 15 m,whilst others in the troop showed affectionate behaviours,gave cohesion calls and displayed ambiguous back-and-forthmovements, switching between following the troop andreturning to the infant, sometimes for hours. Similarly,Santini (2012) observed a dying ring-tailed lemur infantrepeatedly fall, vocalise, and attempt to climb onto theback of its mother, who wavered between staying withthe infant or the group, eventually choosing the latter.Additionally, Littlefield (2010) observed two infanticides insifakas (Propithecus verreauxi) where the females stayed withthe dying infant, occasionally grooming it and, after itsdeath, remaining with the corpse before giving cohesion callsand then following the group. In experimental settings withvarious prosimians, Rosenson (1977) noted that, whilst noneof the mothers attempted to carry their dead infants, all wereobserved to groom them; a galago (Otolemur crassicaudatus)retrieved her infant using her jaws (later and dropping itwhen attempting to groom), and a black lemur (Eulemurmacaco) was seen gripping and lifting her infant. Groomingwas observed in all mothers, most of which were in regularcontact with their infants, likely representing an attemptto elicit a response. While it seems strepsirrhines lack themorphological proficiency for extended periods of carrying,their behaviour suggests they are not indifferent to their deador dying infants, even after they stop showing signs of life(Nakamichi, 2016).