American Journal of Primatology 72:509514 (2010)

RESEARCH ARTICLE Cannibalism in Wild Bonobos (Pan paniscus) at Lui Kotale

ANDREW FOWLER AND GOTTFRIED HOHMANN Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

We describe the cannibalization of an infant bonobo (circa 2.5 years old) at Lui Kotale, in the Democratic Republic of Congo. The infant died of unknown causes and was consumed by several community members including its mother and an older sibling one day after death. Certain features concerning the pattern of consumption t in with previously observed episodes of cannibalism in Pan, whereas others, such as the mothers participation in consuming the body, are notable. The incident suggests that lial cannibalism among apes need not be the result of nutritional or social stress and does not support the idea that lial cannibalism is a behavioral aberration. Am. J. Primatol. 72:509514, 2010. r 2010 Wiley-Liss, Inc. Key words: lial cannibalism; bonobos; Lui Kotale INTRODUCTION Among primates, cannibalism is reported for a diverse range of genera and species including blue monkeys (Cercopithecus mitis stuhlmanni) [Fairgrieve, 1995], red tailed monkeys (Cercopithecus ascanius) [Struhsaker, 1977], red colobus (Piliocolobus badius) [Leland et al., 1984], baboons (Papio ursinus) [Collins et al., 1984], common marmosets (Callithrix jacchus) [Bezerra et al., 2007] and snub-nosed monkeys (Rhinopithecus bieti) [Xiang & Grueter, 2007]. Among hominoids, it has been widely reported among chimpanzees (Pan troglodytes) usually although not exclusively following infanticide [Sherrow & Amsler, 2007], and has been inferred from indirect evidence among gorillas (Gorilla beringei beringei) [Fossey, 1984]. Filial cannibalism (consumption of offspring by parent or parents) has recently been reported from orangutans (Pongo abelii) [Dellatore et al., 2009]. Here we report the rst case of cannibalism observed in a wild community of habituated bonobos. METHODS Observations result from ongoing eld studies of the Bompusa community of bonobos in Lui Kotale, in the Democratic Republic of Congo. The Lui Kotale Bonobo Project was initiated in 2002 and the adult members of the community were habituated to human presence by the time of the presented observations in July 2008. The eld site is located close to the western border of Salonga National Park (South block) and the study site is 25 km away from the nearest village and stretches from the river Lokoro towards the South [Hohmann & Fruth, 2003b]. All members of the Bompusa community have been identied by physical features. The Bompusa community consists of approximately 35 individuals including juveniles and infants. These include ve adult and four sub-adult males, 12 adult and ve sub-adult females. Individuals tolerate follows by groups of researchers and assistants on the ground facilitating long-term observations. Most adult individuals allow observations from distances of 57 m from the observer. Nest party composition and the dynamics of foraging parties are recorded daily and diurnal travel routes are logged using GPS equipment. Individual focal observations are made on adult males and females. The data presented here were recorded by hand ad libitum by Andrew Fowler. The methods used to collect observational data in the eld are in compliance with animal care regulations and with the requirements and guidelines of the Institut Congolaise pour la Conservation de la Nature (ICCN), and adhered to the legal requirements of the host country, the Democratic Republic of Congo. RESULTS The case of cannibalism reported here concerns the infant of an AF (Olga), individually identied in January 2006. At the time the cannibalism occurred,
Contract grant sponsors: Max-Planck-Society; The L.S.B. Leakey Foundation; National Geographic Society; The Volkswagen Foundation; and private donors.
Correspondence to: Andrew Fowler, Department of Primatology, Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig 04103, Germany. E-mail: andrew_fowler@eva.mpg.de

Received 10 June 2009; revised 21 December 2009; revision accepted 25 December 2009 DOI 10.1002/ajp.20802 Published online 21 January 2010 in Wiley InterScience (www. interscience.wiley.com).

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Olga was fully habituated to the presence of researchers and local eld assistants. The female was accompanied by two immature females, assumed to be her daughters, Ophelia (age estimate: 56 years) and Olivia (age estimate: 2.53 years). Olivia was sired by a community member, as conrmed by genetic analysis (personal communicationGrit Schubert, Doctoral student in Department of Primatology, MPI-EVA) and did not show obvious signs of illness or malnutrition. Olga was judged to be peripheral and low-status compared with other females in the community based on her patterns of association. Ophelia was judged to be the daughter of Olga based on constant association and proximity, although this remains an assumption. Due to presumed injury to her right hand resulting in the loss of the three middle ngers, Ophelia seemed unable to travel quadrupedally for long distances, and was frequently carried dorsally by Olga, in addition to her carrying Olivia ventrally. Age estimates for the infants were based on size at rst observation and time since rst observed. Olivia was a young infant in January 2006, and therefore estimated to be between 2 and 3 years old at the time of death. Ophelia was rst observed as a dependent infant carried by Olga in 2004, estimated to have been born in 2002, resulting in an interbirth interval estimated at three years between offspring. This accords with estimates calculated for other females in the community, although precise age estimates are not possible for individuals born before habituation was completed. In the following summary and detailed description of the consumption, relationships between individuals are derived from observation. Females carrying infants are assumed to be the mother in all
TABLE I. Individuals present on 9 and 10 July 2008 Infants Date 9, 10 9, 10 9, 10 9, 10 9, 10 9, 10 9, 10 9 9, 10 10 Date 9, 10 10 Luna Bridget Adult Females (AF) Eva Gwen Hannah Iris Marta Olga Paula Rio Zoe Uma Female (IF) Male (IM) Egon Gustav Hugo Ida

cases, and juveniles in constant close proximity to females are assumed to be their offspring. Table I shows all individuals observed on 9 and 10 July 2008. Abbreviations used in text are shown in Table I. Summary of Events On the morning of July 09, 2008, Olga and Olivia were seen at 06:39 together with Ophelia, having already left their nests. At this time neither female exhibited any obvious signs of injury or ill-health. Olivia was observed to be alive, clinging to Olga and although not moving independently, nothing unusual was noticed in her behavior, since infants may rest or sleep on their mothers without moving. Olga was observed feeding arboreally in close proximity to Iris, another AF with an IF aged approximately two years. Olgas sexual swelling was recorded as stage three out of four, according to the daily protocol. Observers followed group members as they left the feeding tree and travelled terrestrially for approximately 200 m, visiting a second feeding tree. No vocalizations or signs of aggressive behavior were recorded. At 08:00 Olga was seen again, this time carrying the dead body of Olivia. The infants body was exible and rigor mortis was not evident, no signs of injury were noticed. At 08:13 Olga descended to the ground carrying the body around the torso in her right hand and attempted to transport it dorsally. Luna (SAF) groomed the body, and a JM approached and gazed at it intently. At 08:26 Olga ascended and fed in a g tree with other community members, carrying the body in her hand. At 08:43, the feeding party of two AMs and four females, including Olga, descended and were followed on the

Juveniles Female (JF) Male (JM) Date 9, 10 9, 10 9, 10 9 9 Adult Males (AM) Camillo Dante Ben Jack Tito

Moe Olivia Peggy Ophelia Polly Roque Zed Sub-Adult Females (SAF)

Date 9, 10 9, 10 10 9

Sub-Adult Males (SAM) Emil Apollo Pan Max

Infants and juveniles are in row of mothers.

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ground. They were lost at 10:17 and not contacted again that day. The same party was contacted one day later at 07:57 and behavioral interactions involving the dead infant, her mother, and other community members were recorded. During seven and a half hours of observation (07:5715:36) six of the nine AFs present consumed meat, and three gained possession of the carcass for some period. Two of the three AMs also consumed meat and were in possession of the carcass. Possession changed 14 times, including multiple episodes for some individuals including the mother. Interactions with the body took various forms. Marta, a dominant AF physically wrestled it from Olgas possession. Other females and males begged and sometimes obtained meat from the various possessors. Several adult and JMs played with the skin, running and chasing the possessor but without aggression. After most of the softer tissue had been consumed, Olga carried the remains that consisted mainly of skin with one foot and hand attached. Observations on the Day of Consumption The following is a detailed description of events observed by Andrew Fowler and recorded ad libitum on July 10, 2008, the day following the recorded death of the infant. 07:57 Olga was observed travelling arboreally, carrying Olivia in one hand. The body was limp and wet, with the skin on the top of the skull and back exposed. The anal region was swollen and distended. Olga plucked pieces of fur and skin from the infants head and put them in her mouth. 08:16 Genito-Genital (GG) rubbing between Olga and Marta (AF) on the ground. 08:27 Ophelia ((JF), daughter of Olga) groomed Olivia, licking the skin on the babys arm and putting pieces of fur in her mouth. JM touched Olivia. Hannah (AF with IM), Marta (AF with JM) and Zoe (AF with JM) sat around Olga as she groomed the body. Ben (AM) branch-dragged towards the group. GG observed between Olga and Zoe. Ben branch-dragged towards the group. Marta snatched the body from Olga, who relinquished it with slight resistance and sat watching Marta as she examined the body. Marta ran several meters away carrying the body. 08:54 GG Olga and Marta. 08:56 Olga attacked Marta then they both moved out of sight, Marta in possession of the body. 09:02 Marta was observed feeding from the carcass. SAF ate meat. Ben was driven out of the group. GG Olga and Marta. Both fed on meat. 09:15 Zoe observed, but had no meat. Ophelia, Iris (AF with IF), Luna, Marta had meat. Camillo (AM), Moe (JM of Marta) and Dante (AM) remained outside the group with no meat.

Iris and Ophelia had the carcass. 09:27 Copulation between Camillo and Iris. Camillo took the carcass and ran. All followed, including Dante. Olga pulled the body towards her. Dante in possession of a bone. Iris, Dante, Olga, Ophelia and Apollo (SAM) with meat. Ben had carcass. Iris with meat. Dante outside the group. Iris, Marta, Olga, Ben and Hannah with meat. Luna (SAF) fed on meat. Emil (SAM) outside the group. Paula (AF with IF and JF) lying outside without meat. 09:47 Olga with body. Climbed a tree. Dante had meat. Camillo climbed into tree, chased out by Olga. Iris, Hannah, Marta, Olga travelled with the carcass. Uma (AF), Paula and Dante all followed. Apollo had meat. Uma begged but did not receive meat. 10:05 Olga fed on the insides of the body, legs gone. Olga, Ophelia and Luna with body. Camillo followed but without meat. Marta rested without meat. 10:13 GG Olga and Paula. Uma, Ophelia, Olga and Paula with body. 10:14 GG Uma and Olga. Pan (SAM) had meat. 1 vertebra and 2 ribs from body recovered from ground and stored in ethanol. 10:24 Paula and Iris had the body. GG Olga and Polly (JF of Paula). Ophelia ate meat. 10:32 Olga attempted to retrieve the body. Zoe, Zed (JS of Zoe), Ophelia and Olga with meat. 10:35 AM took body into next tree (a distance of less than 50 m), fed on fruit of Botuatope (Landolphia sp.) Ophelia, Uma and unidentied AM with body. 10:45 Large group arrived travelling terrestrially. (Gwen (AF with IM); Eva (AF with IM); Bridget (SAF); Ben; Dante; Camillo; Hannah; Apollo). AM with body. Olga attacked Uma. 10:52 Olga sat alone 5 m above the ground in a tree. AM carried body, followed by Ophelia, Luna and Uma. 11:27 Eva, Emil and Gwen arrived. Emil had a small piece of meat. 11:45 Camillo with carcass. 11:54 Dante obtained meat. Uma, Emil and Egon (infant son of Eva) begged. Emil obtained meat. Camillo with carcass, followed by Ophelia, Olga and unidentied AF. Piece of meat fell to the ground, retrieved by Dante. Skull fell, all descended in pursuit: Olga, Iris, Marta and Dante. Camillo had carcass. Uma, Eva, Marta, Olga, Iris followed. Marta, Olga, Uma, Hannah and Ophelia around Camillo.

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Eva, Emil, Dante and Zoe outside group. 12:25 Marta with body. Uma fed on skull cap. Hannah, Olga, Iris, Marta, Moe, Ophelia and Uma around body, Marta in possession. Hugo (IM of Hannah) with the skull cap. 13:28 Olga wrapped the remains of the body around her neck. 14:01 Bonobos fed on large fruit of Treculia. 14:06 Olga carried skin with one intact foot and one hand still attached Hannah, Eva, Zoe, Uma and Luna followed. 14:10 Ophelia, Olga, Hannah and Bridget fed on carcass. 14:16 Bridget displaced. Hannah with carcass. 14:19 Hannah descended with carcass, Olga followed. 14:23 Hannah descended with skin. Camillo and Ben had meat. Bridget obtained a bone. Dante with meat. Apollo, Hannah, Bridget and Camillo around carcass. Camillo left carrying skin. Dante ate meat with mouthfuls of Treculia. Olga, Zoe, Zed, Ben fed on Treculia. Marta on ground. Camillo had skin, Dante, Apollo ate next to Camillo. Camillo, Moe and Dante fed on Treculia. 14:51 Moe with skin. Skin retrieved by Olga, who draped it over her shoulder. 14:53 Olga lay looking at the skin, looping it through her ngers. 14:54 Bonobos were vocalizing. Olga and Ophelia sat together eating last remnants of esh from skin of Olivia. 14:39 Olga carried skin across shoulders. 15:00 Ophelia chewed on skin, carried it away. Olga joined the group, feeding on Treculia. Ophelia sat alone chewing on skin. Olga, Hannah, Marta, Zoe, Camillo fed on Treculia. Moe begged from Ophelia. Moe feeds with Ophelia. 15:26 Apollo, Hannah fed on Treculia. Camillo played with Ophelia. 15:36 Ben carried skin, dropped it. The remains were not seen again.

DISCUSSION Cannibalism has often been described as the result of aberrant, unnatural behavior induced by overcrowding, stress or individual pathology, [Britz & Pienaar, 1992; Goodall, 1986; Tartabini, 1991]. Dellatore et al. [2009] conclude that environmental stressors are the more likely explanation, arguing against nutritional gain or individual life history, albeit not very strongly. Environmental stressors are more easily imagined in the case of released

rehabilitant orangutans exposed to an unregulated tourism industry than in the case of wild bonobos in a remote location. The case reported on here involved wild bonobos that did not show any signs of behavioral aberration. During the time preceding the death of the infant, no signs of aggressive interactions were recorded, leaving the cause of death to speculation. In the absence of physical injuries the most likely causes of mortality are physical collapse due to disease or as a result of an accident. However, since Olga and Olivia were not always visible to the observers, one cannot exclude that the death was associated with aggressive behaviors by other community members. Observations from Wamba [Kano, 1992] and Lomako [Hohmann & Fruth, 2003a] show that dead infants are often carried by their mothers for several days and that even when the carcass is in an advanced stage of decomposition, mothers treat the dead body as attentively as they do when infants are alive, behavior also noted for other ape mothers, including mountain gorillas [Warren & Williamson, 2004] and chimpanzees [Goodall, 1986]. However, we cannot exclude that other group members did not attempt to take the dead infant away from the mother in these cases. Cannibalism of infant chimpanzees (Pan troglodytes) is a rare but widespread event, usually following infanticide, having been observed at several long-term study sites where the apes are fully habituated to the presence of human observers [Boesch & Boesch-Achermann, 2000; Bygott, 1972; Goodall 1986; Kawanaka, 1981; Reynolds, 2005]. (For more recent reviews: [Murray et al., 2007; Sherrow & Amsler, 2007]). Deaths are often the result of sustained attacks inicting severe and visible wounds, discordant with the lack of such signs on the body of Olivia and a lack of any commotion and vocalizing between the rst sighting of Olga in the morning until her appearance with the dead infant at 8:00. These facts make it unlikely that the death was caused directly by infanticidal behavior. There would seem to be clear potential nutritional benets to consuming the resources available in the form of an infant. The questions to consider are when would it not be benecial to consume the body of a dead baby, and is there any special signicance attached to an infant compared with other nutritional resources. AM polar bears have been reported to predate upon and cannibalize smaller female and younger male conspecics, with an apparently clearly nutritional purpose [Amstrup et al., 2006]. Grizzly bears (Ursus arctos) and black bears (Ursus americanus) have both been recorded as cannibalistic, predating on adult as well as infant conspecics [Tietje et al., 1986], seemingly for nutritional reasons. Rabbits and other rodents may eat their young when mothers are exposed to external stress, and the behavior has been explained

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as over-protection (saving infants by ingesting them) [Labov et al., 1985]. The potential benets to be derived from cannibalism are partially outweighed by the costs of exposure to infectious diseases. Risks to health from cannibalism have been proposed [Pfennig et al., 1998], and experimentally demonstrated. Cannibalistic tiger salamanders (Ambystoma tigrinum) which consumed diseased conspecics were signicantly less likely to survive to metamorphosis and grew signicantly less than those consuming diseased heterospecics, suggesting negative consequences of cannibalism compared with other predatory activity [Pfennig et al., 1999]. If risks to health are pronounced, this suggests that where cannibalism is more common, nutritional stress may be the cause, as in the recently reported cases of predationcannibalism in polar bears [Amstrup et al., 2006]. In some cases, the risks to health outweigh the cost of not utilizing this available food source. Among tiger salamanders survival in rapidly deteriorating environments might be achieved through the rapid growth resulting from predation on conspecics, despite the experimentally demonstrated risks to the health of the cannibals [Pfennig et al., 1999]. Nishimura and Isoda [2004] have modeled the energy gain benets of cannibalism against the attenuating costs of counterattack, concluding that rates of conspecic predator/prey interactions should remain low. Regarding the incidents of lial cannibalism recently reported in orangutans, Dellatore et al. [2009] did not infer infanticide in these cases, and consider nutritional gain (for trace nutrients) or past history explanations, suggesting that the behavior is aberrant. They referred to the individual circumstances of the two mothers: namely that they are wild-born, rehabilitated individuals, whose behavior is likely to have been affected by their social isolation and deprivation. The current observation of lial cannibalism by a wild female bonobo suggests either that such explanations are not necessary, and that this behavior is within the natural repertoire, or else that the behavior of habituated apes is similarly unnatural as a result of the stress of contact with human observers. An interesting aspect of the case of cannibalism reported here is the fact that the body was removed from the mother by a dominant female (Marta) and subsequently consumed by conspecics including the mother. The linear nature of the male hierarchy in the Bompusa community has been established through analysis of patterns of displacement and aggression (unpublished data of Martin Surbeck Doctoral student in the Department of Primatology, MPI-EVA). However, similar patterns of dominance among female bonobos in the community have been less readily discerned empirically. Personal observations (Andrew Fowler) of interactions between Marta

and other females and males, particularly regarding possession of valuable and monopolizable resources such as fruit and meat has indicated her high status, and her centrality in the community. The position of Olga as a lower ranking, more peripheral member of the community is similarly based on observation of interactions between Olga and other community members. GG rubbing between Marta and Olga was observed twice prior to Marta obtaining the body. GG rubbing is common during episodes of meat consumption, and has been observed, for example, after the capture but before the consumption of both monkeys and duikers [Hohmann & Fruth, 1996]. Similarly, while possession of meat is generally respected, changes in ownership do occur, and these are often accompanied by GG rubbing. On several prior occasions, Marta has been observed to monopolize and consume meat resources in the form of duikers, suggesting her high rank, and indicating that female bonobos are able to gain possession of meat and consume it even in the presence of males. It is not known in all cases whether she originally captured the animals, since observations usually begin after capture, which are seldom witnessed, when observers are alerted to the event through duiker distress calls. The signicance of the fact that a more senior and apparently higher ranking female bonobo was able to gain possession by force of the body of another females baby and to start to consume it is open to debate. Biological anthropologists and primatologists have tended to take a somewhat emotive approach to the practice of cannibalism in apes. de Waal and Lanting [1997] for example, suggest; The chimpanzee was the perfect primate example for this time especially after the discovery of intraspecic killing and cannibalism (p 153), explicitly bundling eating with killing where conspecics are concerned. They continue: (Chimpanzee) ymales in the wild engage in brutal warfare against other groups, ythey may kill and cannibalize infants of their own speciesy [de Waal & Lanting, 1997; p 85]. While the case of cannibalism by wild bonobos is likely to remain anecdotal, it shows that the behavioral repertoire of Pan paniscus is still not fully explored. Field studies on this and other populations are likely to reveal behaviors that have not yet been described and will expand our view of the behavioral ecology of P. paniscus. ACKNOWLEDGMENTS Thanks are due to the Institut Congolaise pour la Conservation de la Nature (ICCN) for granting permission to conduct eldwork at Salonga National Park. Sincere thanks go to: the people of Lompole for granting permission to work in their forest; the staff at Lui Kotale for their assistance and cooperation; Barbara Fruth, Caroline Deimel and

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Martin Surbeck for their indispenable contribution to the eldwork; Heidi Douglas for logistical support and Grit Schubert, (Doctoral student in the Department of Primatology, MPI working on population genetics in wild chimpanzees and bonobos) for determining the genetic relatedness of bonobos within and beyond the Bompusa community. Fieldwork at Lui Kotale is supported by the Max-PlanckSociety, The L.S.B. Leakey Foundation, National Geographic Society, The Volkswagen Foundation, and private donors. The methods used to collect observational data in the eld are in compliance with animal care regulations and with the requirements and guidelines of the Institut Congolaise pour la Conservation de la Nature (ICCN), and adhered to the legal requirements of the host country, the Democratic Republic of Congo.

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