Social Grooming Network in Captive Chimpanzees: Does the Wild Or Captive Origin of Group Members Affect Sociality?
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Social grooming network in captive chimpanzees: does the wild or captive origin of group members affect sociality? Marine Levé, Cédric Sueur, Odile Petit, Tetsuro Matsuzawa & Satoshi Hirata Primates ISSN 0032-8332 Primates DOI 10.1007/s10329-015-0494-y 1 23 Your article is protected by copyright and all rights are held exclusively by Japan Monkey Centre and Springer Japan. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Primates DOI 10.1007/s10329-015-0494-y ORIGINAL ARTICLE Social grooming network in captive chimpanzees: does the wild or captive origin of group members affect sociality? 1 2,3 2,3 4,5 Marine Leve´ • Ce´dric Sueur • Odile Petit • Tetsuro Matsuzawa • Satoshi Hirata6 Received: 28 August 2015 / Accepted: 6 September 2015 Ó Japan Monkey Centre and Springer Japan 2015 Abstract Many chimpanzees throughout the world are theoretical removal of individuals from the network had housed in captivity, and there is an increasing effort to differing impacts depending on the origin of the indi- recreate social groups by mixing individuals with captive vidual. Contrary to findings that non-natural early rearing origins with those with wild origins. Captive origins may has long-term effects on physical cognition, living in entail restricted rearing conditions during early infant life, social groups seems to compensate for the negative including, for example, no maternal rearing and a limited effects of non-natural early rearing. Social network anal- social life. Early rearing conditions have been linked with ysis (SNA) and, in particular, theoretical removal analy- differences in tool-use behavior between captive- and sis, were able to highlight differences between individuals wild-born chimpanzees. If physical cognition can be that would have been impossible to show using classical impaired by non-natural rearing, what might be the con- methods. The social environment of captive animals is sequences for social capacities? This study describes the important to their well-being, and we are only beginning results of network analysis based on grooming interac- to understand how SNA might help to enhance animal tions in chimpanzees with wild and captive origins living welfare. in the Kumamoto Sanctuary in Kumamoto, Japan. Grooming is a complex social activity occupying up to Keywords Pan troglodytes Á Social network analysis Á 25 % of chimpanzees’ waking hours and plays a role in Grooming Á Early rearing differences Á Behavioral the emergence and maintenance of social relationships. development Á Well-being We assessed whether the social centralities and roles of chimpanzees might be affected by their origin (captive vs wild). We found that captive- and wild-origin chim- Introduction panzees did not differ in their grooming behavior, but that Due to their phylogenetic similarity to humans, chim- & Satoshi Hirata panzees (Pan troglodytes) have attracted attention from [email protected] both zoos and researchers, and hundreds of individuals have been brought into captivity from their African habitats 1 Ecole normale supe´rieure, Paris, France (Goodall and Peterson 1993). As a social species, chim- 2 De´partement Ecologie, Physiologie et Ethologie, Centre panzees live in groups of several members (Inskipp 2005). National de la Recherche Scientifique, Strasbourg, France Chimpanzee societies, which are known for their com- 3 Institut Pluridisciplinaire Hubert Curien, Universite´ de plexity, are demanding in terms of social cognition. They Strasbourg, Strasbourg, France display fission–fusion dynamics (Aureli et al. 2008), 4 Primate Research Institute, Kyoto University, Aichi, Japan wherein the community splits into smaller subgroups dur- 5 Japan Monkey Centre, Aichi, Japan ing one or even several days (Nishida 1968). Despite this, community cohesion and social bonds among members are 6 Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, 990 Ohtao, Misumi, Uki, Kumamoto 869-3201, maintained. The social network of the community is thus Japan complex (Shimada and Sueur 2014), with some individuals 123 Author's personal copy Primates playing central roles in the collective social life (Kan- different sub-populations, acting as ‘‘brokers’’ and allow- ngiesser et al. 2011). ing the transmission of information among the entire In captivity, group members may arrive from other population (Lusseau et al. 2006). In other studies, the places where they were also captive; they may be born into simulated removal of central individuals from a network in captivity, or they may have come from the wild. The early captivity according to decreasing centrality resulted in rearing of captive infant chimpanzees is not always per- greater network fragmentation and loss of group stability formed by the mother, whereas the infant stays very close than did the removal of random targets (chimpanzees: to its mother for the first 2 or 3 years in the wild (Bard Kanngiesser et al. 2011; mandrills: Bret et al. 2013). 1995). It is thought that normal behavioral development In this study, we assessed whether the grooming depends, in part, on the early circumstances of the infant. behavior and social centrality of 15 chimpanzees differed Severe sensory and social isolation during these formative according to their origin: captive-born vs wild-born. We years results in behavioral consequences, reducing the measured and compared several centrality indices between individuals’ ability to live in social groups, copulate, and wild- and captive-origin members, also considering the raise infants of their own (Bloomsmith et al. 2006). hierarchical rank and age of individuals. We expected Nursery-reared chimpanzees show more frequent abnormal social network centralities to be linked to individual attri- behaviors than their maternally reared counterparts (Ross butes such as age or dominance rank, as shown in Kan- 2003; Bloomsmith and Haberstroh 1995), have reduced ngiesser et al. (2011). On the other hand, we expected to sexual and maternal abilities (Brent et al. 1996), and are observe differences among individuals according to their less likely to reproduce as adults (King and Mellen 1994). origin, with wild-origin chimpanzees showing greater The physical cognition of nursery-reared chimpanzees is social ability with their congeners and displaying higher also impaired: they have reduced problem-solving skills centrality. We anticipated homophily according to origin, (Brent et al. 1995), and seem to show less adaptive with clustering between wild-origin and captive-origin behavior than their wild-born counterparts (Morimura and individuals. Indeed, Massen and Koski (2013) showed that Mori 2010). In addition, this impairment may extend to chimpanzee relationships are based on similarities in social aspects of their behavior, as behaviors such as tool individual characteristics such as personality. We also use use are usually learned through social learning during theoretical methods to remove individuals from the social infancy both in the wild and in captivity (Biro et al. 2003; network and assess the impact of removing either captive- Hirata and Celli 2003; Matsuzawa et al. 2006), and the or wild-born members on group stability and cohesiveness. aggressiveness of offspring is also influenced by the We hypothesized that group stability would also be better aggressiveness of their mothers (Thierry et al. 2004). maintained by wild-origin individuals. The position of an individual in the social network (i.e., centrality) largely determines an individual’s behavior with respect to other members (Sueur et al. 2011a, b). The Methods maintenance of social relationships in a social network through grooming behavior is a time-consuming task and, Subjects and environment if the physical cognition of nursery-reared chimpanzees is impaired, social cognition, particularly the ability to The observed chimpanzees were housed in the Kumamoto develop and maintain relationships, may also be impaired. Sanctuary (KS), Japan, in an all-male captive group of 15 Social network analysis (SNA) tools are also valuable in individuals, seven of whom were of wild origin and eight primate behavioral management: in rhesus macaques of whom were of captive origin (see Morimura et al. 2011 (Macaca mulatta), social network measures were shown to for more information on the facility and its history). The be good predictors of aggressiveness (McCowan et al. captive-born chimpanzees were not all reared maternally. 2008). In chimpanzees, SNA allowed the assessment of Four of them were rejected by their mothers within social preferences in a captive group, validating the use of 4 months of birth and subsequently hand-reared. One a large modern facility where individuals are not forced to individual was separated from its mother at the age of interact (Clark 2011). Using SNA, another study showed 7 months following the breeding policy of the owner that, following the successful integration