Annotated Bibliography

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International Journal of Paleopathology 1 (2011) 128– 129

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International Journal of Paleopathology

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / i j p p

eview

ehavior toward the dying, diseased, or disabled among animals and its elevance to paleopathology

eter J. Fashing ∗, Nga Nguyen epartment of Anthropology and Environmental Studies Program, California State University Fullerton, Fullerton, CA 92834, United States

r t i c l e i n f o

rticle history: eceived 9 February 2012 ccepted 10 February 2012

eywords: hanatology ompassion

a b s t r a c t

Compassionate behavior towards dying, diseased, or disabled 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, we review recent studies of animal behavior toward the dying, diseased, or disabled which may be of interest to paleopathologists and bioarchaeologists studying compassionate behavior in humans and their extinct ancestors. ‘Compassionate’ behavior toward the enfeebled and dying has now been reported in several

eath rieving are giving athology

non-primate mammals (e.g., wild African elephants and river otters) and nonhuman primates (primarily captive chimpanzees). In addition, a number of recent reports have documented wide variation in non- human primates’ reactions to recently deceased group mates (or offspring) both across species, as well as across individuals belonging to the same social group. We suggest there is considerable potential for col- laboration among paleopathologists and primatologists in examining the causes of illness and disability in animals and its impact on their lives.

‘Compassion’ toward dying, diseased, or disabled individuals is egarded as being among the ‘socio-moral’ behaviors that make s human (Counts and Counts, 1991; Keltner et al., 2010). Under- tanding the origins of compassionate behavior is a growing area of nterest in several subfields of evolutionary anthropology, includ- ng bioarchaeology and paleopathology (e.g., Hawkey, 1998; Tilley nd Oxenham, 2011). Although controversial, the earliest evi- ence from the fossil record of compassion toward the dying, iseased, or disabled appears 1.8 million years ago (Hublin, 2009; ordkipanidze et al., 2005). While studying the fossil record is a ey avenue for evaluating the evolution and relative uniqueness f human compassion, another promising route is to examine the ehavior of nonhuman primates and other animals for evidence f compassionate behavior toward enfeebled family members or roup mates. By adopting a comparative evolutionary approach oward compassionate behavior among animals, the timing of the volution of various behaviors, and the number of times they volved independently, can be estimated. Although long confined rimarily to rare, isolated accounts (e.g., Cowgill, 1972; Nakamichi t al., 1996), the literature on animal behavior toward infirm group

ates has expanded rapidly, especially among our closest relatives,

himpanzees, over the past several years. Here, we briefly review he findings from several journals which have recently featured

∗ Corresponding author. Tel.: +1 657 278 3977; fax: +1 657 278 5001. E-mail address: [email protected] (P.J. Fashing).

879-9817/$ – see front matter © 2012 Elsevier Inc. All rights reserved. oi:10.1016/j.ijpp.2012.02.004

© 2012 Elsevier Inc. All rights reserved.

articles focusing on animal behavior toward the dying, diseased, or disabled which may be of interest to paleopathologists studying compassionate behavior in humans and their ancestors.

Several of the most striking recent examples of compassionate behavior toward the enfeebled and dying come from non-primate mammals, emphasizing the importance of caution in making claims about human or primate exceptionalism. In Applied Animal Behaviour Science, Douglas-Hamilton et al. (2006) recently provided a detailed account of the last days of a dying African elephant (Loxodonta africana) matriarch at Samburu, Kenya. Struggling to stand upright and left behind by her own fellow group mem- bers, the dying female was approached by the matriarch of another group who repeatedly attempted to bring her to her feet using her tusks. Perplexingly, while the ‘compassionate’ matriarch was clearly stressed, other members of the ‘compassionate’ matriarch’s group exhibited no interest in the dying female. Douglas-Hamilton et al.’s (2006) observations suggest that individual African ele- phants vary in the extent to which they exhibit compassion toward enfeebled individuals, a pattern also characteristic of humans (Keltner et al., 2010). Another intriguing recent study in PLoS One (Davenport, 2010) reported how an elderly river otter (Pteronura brasiliensis) matriarch with failing vision and poor mobility was kept alive in a Peruvian oxbow lake for many months through pro-

visioning with pieces of large fish caught by other members of her group. This study represents one of the only documented examples among nonhuman animals of younger individuals transferring food to elderly group members.

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Recent video footage and an accompanying paper in Current iology by Anderson et al. (2010) focusing on observations of cap- ive chimpanzees (Pan troglodytes) created a flurry of interest in ehavior toward dying individuals in nonhuman primates. In this aper, Anderson et al. (2010) describe the remarkably compassion- te care directed toward a dying older female chimpanzee by her roup mates, who groomed and caressed her for hours as she lay ying in an indoor enclosure at Blair Drummond Safari Park in cotland.

Inspired by Anderson et al.’s (2010) paper, a comparative evo- utionary discussion of dying and death among primates has ince continued in the American Journal of Primatology which is ast becoming the journal of choice for publications describing dvances in ‘primate thanatology’. For example, Fashing et al. 2011) described how, unlike Anderson et al.’s (2010) chimpanzees,

embers of a wild gelada (Theropithecus gelada) group, and the erd in which it was traveling, abandoned two group mates, a ick and dying adult female and her seven-month old dependent nfant, when they fell behind. Over the next two days, the female nd subsequently her infant both died, without any members of heir herd returning to search for them. Similarly, Stewart et al. 2012) reported that among wild chimpanzees at Gombe, Tanzania,

dying female spent her last several days in a mostly solitary state, he authors making no mention of compassionate behaviors hav- ng been directed toward the female by others during this period. hese field studies raise the possibility that wild primates, including himpanzees, do not exhibit the same levels of compassion as cap- ive chimpanzees or even, more perplexingly, as wild giant otters nd African elephants, animals far less closely related to humans.

Although perhaps less directly related to paleopathology, many f these same journals have also recently featured articles of poten- ial interest to funerary archaeologists and taphonomists focusing n the extremely variable responses of nonhuman primates to the odies of recently deceased individuals. Reactions by conspecifics o recently dead group mates (or offspring) appear to vary widely cross primate species, as well as across individuals belonging to he same social group. Interested readers are encouraged to consult rticles in Current Biology by Biro et al. (2010), American Journal of rimatology by Cronin et al. (2011), and Anthropological Science by ugiyama et al. (2009), the latter representing an excellent exam- le of a long-term study quantifying the rate and length of carrying f infants after death by their mothers. Of course, it is important to ote that primates are not alone in their interest in investigating he bodies and even the bones of the dead, as recent papers about frican elephants in Biology Letters (McComb et al., 2006) and Neu- oscience and Biobehavioral Reviews (Hart et al., 2008) remind us. nderson (2011) also published a useful commentary in the Amer-

can Journal of Primatology offering a ‘primatological perspective n death’ emphasizing unanswered questions relating to aware- ess of death among primates. Here, we also wish to emphasize he importance of obtaining a comparative evolutionary perspec- ive on primate compassion toward dying, diseased, or disabled ndividuals focusing on as diverse an array of species and popula- ions as possible. Indeed, recent evidence from paleoanthropology ndicates that inferences into the evolution of human behavior ased solely on a chimpanzee model are less informative than reviously believed (Lovejoy, 2009), suggesting that by adopting

broader, more comparative view of primate adaptations, we may ain greater insights into the evolutionary roots of human behavior.

The recovery of the remains of individuals after death enables

dentification of any diseases or disabilities afflicting these indi- iduals and which may have contributed to their deaths. Such emains are especially useful when they come from individuals ith known life histories from intensive behavioral study (e.g.,

l of Paleopathology 1 (2011) 128– 129 129

McFarlin et al., 2009, 2011). Several long-term behavioral field stud- ies of primates have begun to more carefully collect and curate dead individuals, entering into collaborations with museums and their scientific personnel in habitat countries. Of course, to avoid disrupt- ing the natural behavior of the study animals, fieldworkers must take care not to recover individuals until they have been abandoned completely, an event which may not take place for several weeks after death among individuals of some species (e.g., Biro et al., 2010; Fashing et al., 2011). Clearly, there is considerable poten- tial for collaboration among paleopathologists and primatologists in examining the causes of illness and disability in study animals and its impact on their lives.

Acknowledgements

We thank Margaret Judd for inviting us to contribute this review.

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Anderson, J.R., Gillies, A., Lock, L.C., 2010. Pan thanatology. Current Biology 20, R349–R351.

Biro, D., Humle, T., Koops, K., Souse, C., Hayashi, M., Matsuzawa, T., 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20, R351–R352.

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