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Social grooming network in captive chimpanzees: does the wild or captive origin of group members affect sociality?

Primates volume 57, pages 73–82 (2016)Cite this article

Abstract

Many chimpanzees throughout the world are housed in captivity, and there is an increasing effort to recreate social groups by mixing individuals with captive origins with those with wild origins. Captive origins may entail restricted rearing conditions during early infant life, including, for example, no maternal rearing and a limited social life. Early rearing conditions have been linked with differences in tool-use behavior between captive- and wild-born chimpanzees. If physical cognition can be impaired by non-natural rearing, what might be the consequences for social capacities? This study describes the results of network analysis based on grooming interactions in chimpanzees with wild and captive origins living in the Kumamoto Sanctuary in Kumamoto, Japan. Grooming is a complex social activity occupying up to 25 % of chimpanzees’ waking hours and plays a role in the emergence and maintenance of social relationships. 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 chimpanzees did not differ in their grooming behavior, but that theoretical removal of individuals from the network had differing impacts depending on the origin of the individual. Contrary to findings that non-natural early rearing has long-term effects on physical cognition, living in social groups seems to compensate for the negative effects of non-natural early rearing. Social network analysis (SNA) and, in particular, theoretical removal analysis, were able to highlight differences between individuals that would have been impossible to show using classical methods. The social environment of captive animals is important to their well-being, and we are only beginning to understand how SNA might help to enhance animal welfare.

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References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266

    PubMed  CAS  Article  Google Scholar 

  • Asher L, Collins LM, Ortiz-Pelaez A, Drewe JA, Nicol CJ, Pfeiffer DU (2009) Recent advances in the analysis of behavioural organization and interpretation as indicators of animal welfare. J R Soc Interface 6(41):1103–1119

    PubMed  PubMed Central  Article  Google Scholar 

  • Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J, Chapman CA, Van Schaik CP (2008) Fission–fusion dynamics. Curr Anthropol 49:627–654

    Article  Google Scholar 

  • Bard KA (1995) Parenting in primates. In: Bornstein M (ed) Handbook of parenting: biology and ecology of parenting, vol 2. Lawrence Erlbaum Associates, London, pp 27–58

    Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Paper presented at the 3rd international AAAI conference on weblogs and social media, San Jose, California

  • Berry KJ, Mielke PW Jr (2000) Exact and Monte Carlo resampling procedures for the Wilcoxon–Mann–Whitney and Kruskal–Wallis tests. Percept Mot Skills 91:749–754

    PubMed  CAS  Article  Google Scholar 

  • Biro D, Inoue-Nakamura N, Tonooka R, Yamakoshi G, Sousa C, Matsuzawa T (2003) Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments. Anim Cogn 6:213–223

    PubMed  Article  Google Scholar 

  • Bloomsmith MA, Haberstroh MD (1995) Effect of early social experience on the expression of abnormal behavior among juvenile chimpanzees. Am J Primatol 36:11

    Google Scholar 

  • Bloomsmith MA, Baker KC, Ross SR, Lambeth SP (2006) Early rearing conditions and captive chimpanzee behavior: some surprising findings. In: Sackett GP, Elias K (eds) Nursery rearing of nonhuman primates in the 21st century. Springer, New York, pp 289–312

    Chapter  Google Scholar 

  • Borgatti SP, Everett MG, Freeman LC (2002) Ucinet for Windows: software for social network analysis. Analytic Technologies, Harvard, MA

  • Brent L, Bloomsmith MA, Fisher SD (1995) Factors determining tool-using ability in two captive chimpanzee (Pan troglodytes) colonies. Primates 36:265–274

    Article  Google Scholar 

  • Brent L, Williams-Blangero S, Stone AM (1996) Evaluation of the chimpanzee breeding program at the Southwest Foundation for Biomedical Research. Lab Amin Sci 46:405–409

    CAS  Google Scholar 

  • Bret C, Sueur C, Ngoubangoye B, Verrier D, Deneubourg JL, Petit O (2013) Social structure of a semi-free ranging group of mandrills (Mandrillus sphinx): a social network analysis. PLoS One 8:e83015

    PubMed  PubMed Central  Article  Google Scholar 

  • Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469

    Article  Google Scholar 

  • Carlsen F, de Jongh T (2007) European studbook for the chimpanzee Pan troglodytes. Copenhagen Zoo, Roskildevej

    Google Scholar 

  • Clark FE (2011) Space to choose: network analysis of social preferences in a captive chimpanzee community, and implications for management. Am J Primatol 73:748–757

    PubMed  Article  Google Scholar 

  • Cronin KA, Van Leeuwen EJ, Vreeman V, Haun DB (2014) Population-level variability in the social climates of four chimpanzee societies. Evol Hum Behav 35(5):389–396

    Article  Google Scholar 

  • De Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55:827–843

    PubMed  Article  Google Scholar 

  • Dufour V, Sueur C, Whiten A, Buchanan-Smith HM (2011) The impact of moving to a novel environment on social networks, activity and wellbeing in two New World primates. Am J Primatol 73:802–811

    PubMed  CAS  Article  Google Scholar 

  • Fedurek P, Dunbar RI (2009) What does mutual grooming tell us about why chimpanzees groom? Ethology 115:566–575

    Article  Google Scholar 

  • Fedurek P, Machanda ZP, Schel AM, Slocombe KE (2013) Pant hoot chorusing and social bonds in male chimpanzees. Anim Behav 86:189–196

    Article  Google Scholar 

  • Flack JC, Girvan M, De Waal FB, Krakauer DC (2006) Policing stabilizes construction of social niches in primates. Nature 439:426–429

    PubMed  CAS  Article  Google Scholar 

  • Gilby IC, Wrangham RW (2008) Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. Behav Ecol Sociobiol 62:1831–1842

    Article  Google Scholar 

  • Good PI (2005) Permutation, parametric and bootstrap tests of hypotheses, vol 3. Springer, New York

    Google Scholar 

  • Goodall J, Peterson D (1993) Visions of Caliban: on chimpanzees and people. University of Georgia Press, Athens, GA

  • Hemelrijk CK (1990) A matrix partial correlation test used in investigations of reciprocity and other social interaction patterns at group level. J Theor Biol 143:405–420

    Article  Google Scholar 

  • Hirata S, Celli ML (2003) Role of mothers in the acquisition of tool-use behaviours by captive infant chimpanzees. Anim Cogn 6:235–244

    PubMed  Article  Google Scholar 

  • Hothorn T, Everitt BS (2014) A handbook of statistical analyses using R. Chapman and Hall/CRC, London

  • Inskipp T (2005) Chimpanzee (Pan troglodytes). In: Caldecott JO, Miles, L (eds) World Atlas of Great Apes and their Conservation, University of California Press, Oakland, pp 53–81

  • Kanngiesser P, Sueur C, Riedl K, Grossmann J, Call J (2011) Grooming network cohesion and the role of individuals in a captive chimpanzee group. Am J Primatol 73:758–767

    PubMed  Article  Google Scholar 

  • Kawanaka K (1989) Age differences in social interactions of young males in a chimpanzee unit-group at the Mahale Mountains National Park, Tanzania. Primates 30:285–305

    Article  Google Scholar 

  • King NE, Mellen JD (1994) The effects of early experience on adult copulatory behavior in zoo-born chimpanzees (Pan troglodytes). Zoo Biol 13:51–59

    Article  Google Scholar 

  • Koene P, Ipema B (2014) Social networks and welfare in future animal management. Animals 4(1):93–118

    PubMed  PubMed Central  Article  Google Scholar 

  • Lusseau D (2003) The emergent properties of a dolphin social network. Proc R Soc Lond B 270:S186–S188

    Article  Google Scholar 

  • Lusseau D, Newman ME (2004) Identifying the role that animals play in their social networks. Proc R Soc Lond B 271:S477–S481

    Article  Google Scholar 

  • Lusseau D, Wilson BEN, Hammond PS, Grellier K, Durban JW, Parsons KM, Barton TR, Thompson PM (2006) Quantifying the influence of sociality on population structure in bottlenose dolphins. J Anim Ecol 75:14–24

    PubMed  Article  Google Scholar 

  • Majolo B, de Bortoli Vizioli A, Schino G (2008) Costs and benefits of group living in primates: group size effects on behaviour and demography. Anim Behav 76:1235–1247

    Article  Google Scholar 

  • Manno TG (2008) Social networking in the Columbian ground squirrel, Spermophilus columbianus. Anim Behav 75:1221–1228

    Article  Google Scholar 

  • Massen JJ, Koski SE (2013) Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav 35:1–8

    Article  Google Scholar 

  • Matsuzawa T, Tomonaga M, Tanaka M (2006) Cognitive development in chimpanzees. Springer, Tokyo

    Book  Google Scholar 

  • McCowan B, Anderson K, Heagarty A, Cameron A (2008) Utility of social network analysis for primate behavioral management and well-being. Appl Anim Behav Sci 109:396–405

    Article  Google Scholar 

  • Morimura N, Mori Y (2010) Effects of early rearing conditions on problem-solving skill in captive male chimpanzees (Pan troglodytes). Am J Primatol 72:626–633

    PubMed  Google Scholar 

  • Morimura N, Gen’ichi I, Matsuzawa T (2011) The first chimpanzee sanctuary in Japan: an attempt to care for the “surplus” of biomedical research. Am J Primatol 73:226–232

    PubMed  Article  Google Scholar 

  • Newman MEJ (2004) Analysis of weighted networks. Phys Rev E 70:056131

    CAS  Article  Google Scholar 

  • Newman ME (2006) Modularity and community structure in networks. Proc Nat Acad Sci 103:8577–8582

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  • Nishida T (1968) The social group of wild chimpanzees in the Mahali Mountains. Primates 9:167–224

    Article  Google Scholar 

  • Ross SR (2003) The effects of early rearing condition on the social behavioral development of captive chimpanzees (Pan troglodytes). Master’s Thesis, Department of Social Sciences, University of Chicago

  • Rushmore J, Caillaud D, Hall RJ, Stumpf RM, Meyers LA, Altizer S (2014) Network-based vaccination improves prospects for disease control in wild chimpanzees. J R Soc Interface 11:20140349

    PubMed  PubMed Central  Article  Google Scholar 

  • Schel A, Rawlings B, Claidiere N, Wilke C, Wathan J, Richardson J, Slocombe K (2013) Network analysis of social changes in a captive chimpanzee community following the successful integration of two adult groups. Am J Primatol 75:254–266

    PubMed  Article  Google Scholar 

  • Shimada M, Sueur C (2014) The importance of social play network for infant or juvenile wild chimpanzees at Mahale Mountains National Park, Tanzania. Am J Primatol 76:1025–1036

    PubMed  Article  Google Scholar 

  • Sueur C, Pelé M (2015) Utilisation de L’analyse Des Réseaux Sociaux Dans La Gestion Des Animaux Maintenus En Captivité. Analyse des réseaux sociaux appliquée à l’éthologie et à l’écologie. Editions Matériologiques, Paris, pp 445–468

    Google Scholar 

  • Sueur C, Deneubourg JL, Petit O, Couzin ID (2011a) Group size, grooming and fission in primates: a modelling approach based on group structure. J Theor Biol 273:156–166

    PubMed  Article  Google Scholar 

  • Sueur C, Jacobs A, Amblard F, Petit O, King A (2011b) How can social network analysis improve the study of primate behavior? Am J Primatol 73:703–719

    PubMed  Article  Google Scholar 

  • Thierry B, Singh M, Kaumanns W (2004) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, UK

  • Van Leeuwen EJ, Cronin KA, Schütte S, Call J, Haun DB (2013) Chimpanzees (Pan troglodytes) flexibly adjust their behaviour in order to maximize payoffs, not to conform to majorities. PLoS One 8:e80945

    PubMed  PubMed Central  Article  Google Scholar 

  • Watson SK, Townsend SW, Schel AM, Wilke C, Wallace EK, Cheng L, West V, Slocombe KE (2015) Vocal learning in the functionally referential food grunts of chimpanzees. Curr Biol 25(4):495–499

    PubMed  CAS  Article  Google Scholar 

  • Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765–778

    Article  Google Scholar 

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Acknowledgments

We thank all the caretakers at the KS, particularly Michael Seres, for their cooperation and assistance. CS gratefully acknowledges the support of both the University of Strasbourg Institute for Advanced Study (USIAS) and the Fyssen Foundation. This study was funded by JSPS KAKENHI Grant Numbers 25119008 and 26245069, MEXT KAKENHI Grant Number 24000001, JSPS-LGP-U04, and MEXT-PRI-Human Evolution. Our animal husbandry and research practices complied with international standards and were in accordance with the recommendations of the Weatherall report on the use of non-human primates in research as well the guidelines issued by the Primate Society of Japan. The study protocol was approved by the Animal Experimentation Committee of the Wildlife Research Center, Kyoto University (No. WRC-2014KS001A).

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Authors and Affiliations

  1. Ecole normale supérieure, Paris, France

    Marine Levé

  2. Département Ecologie, Physiologie et Ethologie, Centre National de la Recherche Scientifique, Strasbourg, France

    Cédric Sueur & Odile Petit

  3. Institut Pluridisciplinaire Hubert Curien, Université de Strasbourg, Strasbourg, France

    Cédric Sueur & Odile Petit

  4. Primate Research Institute, Kyoto University, Aichi, Japan

    Tetsuro Matsuzawa

  5. Japan Monkey Centre, Aichi, Japan

    Tetsuro Matsuzawa

  6. Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, 990 Ohtao, Misumi, Uki, Kumamoto, 869-3201, Japan

    Satoshi Hirata

Authors
  1. Marine Levé
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  2. Cédric Sueur
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  3. Odile Petit
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  4. Tetsuro Matsuzawa
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  5. Satoshi Hirata
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Correspondence to Satoshi Hirata.

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Levé, M., Sueur, C., Petit, O. et al. Social grooming network in captive chimpanzees: does the wild or captive origin of group members affect sociality?. Primates 57, 73–82 (2016). https://doi.org/10.1007/s10329-015-0494-y

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  • DOI: https://doi.org/10.1007/s10329-015-0494-y

Keywords

  • Pan troglodytes
  • Social network analysis
  • Grooming
  • Early rearing differences
  • Behavioral development
  • Well-being