Advertisement

Primates

, Volume 60, Issue 3, pp 191–202 | Cite as

Comparative social grooming networks in captive chimpanzees and bonobos

  • Michelle A. RodriguesEmail author
  • Emily R. Boeving
Special Feature: Original Article Social networks analysis in primates, a multilevel perspective

Abstract

Despite similar dispersal patterns, models of Pan sociality emphasize sex differences in social bonding between the two species. Such disparities are attributed to hypothesized differences in environmental selective pressures that structure association patterns. However, recent research documents greater within-species variation in social bonds in both species. Here, we examine grooming networks in captive chimpanzees at the North Carolina Zoo, and captive bonobos at the Columbus Zoo. We hypothesized that male–female grooming relationships would be the strongest in both species, but that males and females of both species would not significantly differ between centrality, strength, or clustering. Via Mantel tests, we found that neither bonobos (t = − 0.070, r = − 0.009, two-tailed p = 0.942) nor chimpanzees (t = − 0.495, r = − 0.0939, two-tailed p = 0.6205) had significant differences in grooming between or within sexes. Neither species had significant sex differences in centrality, strength, or clustering. To account for idiosyncratic factors affecting grooming distribution, we examined the effect of origin, kinship, and group tenure on social network position. We found that wild-born bonobos exhibited greater eigenvector centrality (t = − 2.592, df = 9, p = 0.29) and strength (t = − 2.401; df = 9, p = 0.040), and group tenure was significantly correlated with strength (r = 0.608; N = 11, p − 0 = 0.47). None of these factors varied with social network position in chimpanzees. Our findings suggest that in captive settings, idiosyncratic factors related to individual history play a greater role in structuring social networks. Such variation may point to the behavioral flexibility inherent in fission–fusion networks, and mirror between-site variation found in wild chimpanzees. However, some idiosyncratic factors shaping captive networks may be an artifact of captivity.

Keywords

Grooming Social networks Pan Chimpanzees Bonobos 

Notes

Acknowledgements

We appreciate the role of the staff of the Columbus Zoo and Aquarium and the North Carolina Zoo in facilitating this research and their diligent care of the bonobos and chimpanzees. Specifically, we are grateful to Audra Meinelt and the keeper staff at the Columbus Zoo, and Corinne Kendall, Richard Bergl, Jennifer Ireland, and the keeper staff at the North Carolina Zoo. Additionally, we appreciate the work that Steve Ross and the Chimpanzee Species Survival Plan put into reviewing the proposed research and facilitating high chimpanzee welfare standards. We also appreciate discussions with Jessica Walz, Anna Kordek, Dawn Kitchen, Monique Fortunato, Colin Brand, and Ashley Edes in the development of this project. This manuscript was strengthened by the helpful commentary from anonymous reviewers.

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behavior 49:227–267CrossRefGoogle Scholar
  2. Aureli F, Schaffner C, Boesch C, Bearder S, Call J, Chapman C, Connor R, Di Fiore A, Dunbar RIM, Henzi SP et al (2008) Fission–fusion dynamics: new research frameworks. Curr Anthropol 49:627–654Google Scholar
  3. Baker K, Smuts B (1994) Social relationships of female chimpanzees: diversity between captive groups. In: Wrangham R, McGrew W, de Waal F, Heltne P (eds) Chimpanzee Cultures. Harvard University Press, Cambridge, pp 227–243Google Scholar
  4. Barrat A, Barthelemy M, Pastor-Satorras R, Vespignani A (2004) The architecture of complex weighted networks. Proc Natl Acad Sci 101:3747–3752CrossRefGoogle Scholar
  5. Beck B, Walkup K, Rodrigues M, Unwin S, Travis D, Stoinski T (2007) Best practice guidelines for the reintroduction of great apes. IUCN/Primate Specialist Group, Gland, Switzerland, pp 1–48Google Scholar
  6. Boose KJ, White FJ, Meinelt A (2013) Sex differences in tool use acquisition in bonobos (pan paniscus). Am J Primatol 75:917–926CrossRefGoogle Scholar
  7. Brand CM, Marchant LF (2015) Hair plucking in captive bonobos (Pan paniscus). Appl Anim Behav Sci 171:192–196CrossRefGoogle Scholar
  8. Brent LJN, Lehmann J, Ramos-Fernández G (2011) Social network analysis in the study of nonhuman primates: a historical perspective. Am J Primatol 73:720–730CrossRefGoogle Scholar
  9. Chapman CA (1990) Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409–414CrossRefGoogle Scholar
  10. Chapman CA, Chapman LJ, Wrangham R (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70CrossRefGoogle Scholar
  11. Clark FE (2011) Space to choose: network analysis of social preferences in a captive chimpanzee community, and implications for management. Am J Primatol 73:748–757CrossRefGoogle Scholar
  12. Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  13. Dunbar RIM (1976) Some aspects of research design and their implications in the observational study of behaviour. Behaviour 58:78–98CrossRefGoogle Scholar
  14. Dunbar R (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–131CrossRefGoogle Scholar
  15. Fedurek P, Dunbar RIM (2009) What does mutual grooming tell us about why chimpanzees groom? Ethology 115:566–575CrossRefGoogle Scholar
  16. Fortunato M (2009) Dominance style in captive, fission-fusioned bonobos (Pan paniscus): dominance hierarchy, aggressive patterns, and conflict management. PhD Diss. Available from: proquest: 3342098Google Scholar
  17. Freeman HD, Ross SR (2014) The impact of atypical early histories on pet or performer chimpanzees. PeerJ 2:e579CrossRefGoogle Scholar
  18. Freeman HD, Weiss A, Ross SR (2016) Atypical early histories predict lower extraversion in captive chimpanzees. Dev Psychobiol 58:519–527CrossRefGoogle Scholar
  19. Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 18:855–875CrossRefGoogle Scholar
  20. Furuichi T, Ihobe H (1994) Variation in male relationships in bonobos and chimpanzees. Behaviour 130:211–228CrossRefGoogle Scholar
  21. Gersick AS, Rubenstein DI (2017) Physiology modulates social flexibility and collective behaviour in equids and other large ungulates. Philos Trans R Soc B Biol Sci 372:20160241CrossRefGoogle Scholar
  22. Goodall J (1986) The Chimpanzees of Gombe: Patterns of Behavior. Bellknap Press, CambridgeGoogle Scholar
  23. Hare B, Wobber V, Wrangham R (2012) The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. Anim Behav 83:573–585CrossRefGoogle Scholar
  24. Hashimoto C, Furuichi T (2015) Sex differences in ranging and association patterns in chimpanzees in comparison with bonobos. In: Furuichi T, Yamagiwa J, Aureli F (eds) Dispersing Primate Females: Life History and Social Strategies in Male-Philopatric Species. Tokyo, Springer Japan, pp 105–126CrossRefGoogle Scholar
  25. Hashimoto C, Suzuki S, Takenoshita Y, Yamagiwa J, Kanyunyi Basabose A, Furuichi T (2003) How fruit abundance affects the chimpanzee party size: a comparison between four study sites. Primates 44:77–81Google Scholar
  26. Heilbronner SR, Rosati AG, Stevens JR, Hare B, Hauser MD (2008) A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biol Lett 4:246–249CrossRefGoogle Scholar
  27. Hemelrijk CK (1990a) Models of and tests for reciprocity and exchange at a group level. Anim Behav 39:1013–1029CrossRefGoogle Scholar
  28. Hemelrijk CK (1990b) A matrix partial correlation test used in investigations of reciprocity and other social interaction patterns at group level. Anim Behav 39:1013–1029CrossRefGoogle Scholar
  29. Henzi SP, Lycett JE, Weingrill T (1997) Cohort size and the allocation of social effort by female mountain baboons. Anim Behav 54:1235–1243CrossRefGoogle Scholar
  30. Hockings KJ, Anderson JR, Matsuzawa T (2012) Socioecological adaptations by chimpanzees, Pan troglodytes verus, inhabiting an anthropogenically impacted habitat. Anim Behav 83:801–810CrossRefGoogle Scholar
  31. Hohmann G, Fruth B (2000) Use and function of genital contacts among female bonobos. Anim Behav 60:107–120CrossRefGoogle Scholar
  32. Hohmann G, Gerloff U, Tautz D, Fruth B (1999) Social bonds and genetic ties: kinship, association, and affiliation in a community of bonobos (Pan paniscus). Behaviour 136:1219–1235CrossRefGoogle Scholar
  33. Holme P, Min Park S, Kim BJ, Edling CR (2007) Korean university life in a network perspective: dynamics of a large affiliation network. Phys A Stat Mech its Appl 373:821–830CrossRefGoogle Scholar
  34. Itoh N, Nishida T (2007) Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates 48:87–96CrossRefGoogle Scholar
  35. Kahlenberg SM, Emery Thompson M, Wrangham RW (2008) Female competition over core areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda. Int J Primatol 29:931–947CrossRefGoogle Scholar
  36. 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 73:758–767CrossRefGoogle Scholar
  37. Kerth G, Perony N, Schweitzer F (2011) Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proc R Soc B Biol Sci 278:2761–2767CrossRefGoogle Scholar
  38. Lehmann J, Boesch C (2005) Bisexually bonded ranging in chimpanzees (Pan troglodytes verus). Behav Ecol Sociobiol 57:525–535CrossRefGoogle Scholar
  39. Lehmann J, Boesch C (2008) Sexual differences in chimpanzee sociality. Int J Primatol 29:65–81CrossRefGoogle Scholar
  40. Lehmann J, Boesch C (2009) Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. Anim Behav 77:377–387CrossRefGoogle Scholar
  41. Lehmann J, Korstjens AH, Dunbar RIM (2007) Fission–fusion social systems as a strategy for coping with ecological constraints: a primate case. Evol Ecol 21:613–634CrossRefGoogle Scholar
  42. Leve M, Sueur C, Petit O, Matsuzawa T, Hirata S (2016) Social grooming network in captive chimpanzees: does the wild or captive origin of group members affect sociality? Primates 57:73–82CrossRefGoogle Scholar
  43. Lonsdorf EV, Anderson KE, Stanton MA, Shender M, Heintz MR, Goodall J, Murray CM (2014) Boy will be boys: sex differences in wild infant chimpanzee social interactions. Anim Behav 88:79–83CrossRefGoogle Scholar
  44. Lusseau D, Newman MEJ (2004) Identifying the role that animals play in their social networks. Proc R Soc B Biol Sci 271:S477–S481CrossRefGoogle Scholar
  45. Lusseau D, Whitehead H, Gero S (2008) Incorporating uncertainty into the study of animal social networks. Anim Behav 75:1809–1815CrossRefGoogle Scholar
  46. 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 76:1235–1247CrossRefGoogle Scholar
  47. Manson JH, Navarrete CD, Silk JB, Perry S (2004) Time-matched grooming in female primates? New analyses from two species. Anim Behav 67:493–500CrossRefGoogle Scholar
  48. Martin JS, Suarez SA (2017) Personality assessment and model comparison with behavioral data: a statistical framework and empirical demonstration with bonobos (Pan paniscus). Am J Primatol 79(8):e22670CrossRefGoogle Scholar
  49. Massen JJM, Koski SE (2014) Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav 35:1–8CrossRefGoogle Scholar
  50. Matsumoto-Oda A, Hosaka K, Huffman MA (1998) Factors affecting party size in chimpanzees of the Mahale Mountains. Int J Primatol 19:999–1011CrossRefGoogle Scholar
  51. Moscovice LR, Douglas PH, Martinez-Iñigo L, Surbeck M, Vigilant L, Hohmann G (2017) Stable and fluctuating social preferences and implications for cooperation among female bonobos at LuiKotale, Salonga National Park, DRC. Am J Phys Anthropol 163:158–172CrossRefGoogle Scholar
  52. Mulavwa M, Furuichi T, Yangozene K, Motema-salo B, Idani G, Ihobe H, Yamba-Yamba M, Motema-Salo M, Idani G, Ihobe H, Hashimoto C, Tashiro Y, Mwanza N (2008) Seasonal changes in fruit production and party size of bonobos at Wamba. In: Furuichi T, Thompson J (eds) The Bonobos: Behavior, Ecology & Conservation. Springer, New York, pp 121–135CrossRefGoogle Scholar
  53. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045CrossRefGoogle Scholar
  54. Newman MEJ (2001) The structure of scientific collaboration networks. Proc Natl Acad Sci U S A 98:404–409CrossRefGoogle Scholar
  55. Newman MEJ (2004) Analysis of weighted networks. Phys Rev 70:056131Google Scholar
  56. Nishida T (1988) Development of social grooming between mother and offspring in wild chimpanzees. Folia Primatol 50:109–123CrossRefGoogle Scholar
  57. Otali E, Gilchrist JS (2005) Why chimpanzee (Pan troglodytes schweinfurthii) mothers are less gregarious than nonmothers and males: the infant safety hypothesis. Behav Ecol Sociobiol 59:561–570CrossRefGoogle Scholar
  58. Pace DS, Pulcini M, Triossi F (2012) Anthropogenic food patches and association patterns of Tursiops truncatus at Lampedusa Island, Italy. Behav Ecol 23:254–264CrossRefGoogle Scholar
  59. Palagi E (2006) Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): implications for natural social systems and interindividual relationships. Am J Phys Anthropol 129:418–426CrossRefGoogle Scholar
  60. Parish AR (1994) Sex and food control in the “uncommon chimpanzee”: how bonobo females overcome a phylogenetic legacy of male dominance. Ethol Sociobiol 15:157–179CrossRefGoogle Scholar
  61. Parish AR (1996) Female relationships in bonobos (Pan paniscus): evidence for bonding, cooperation, and female dominance in a male-philopatric species. Hum Nat 7:61–96Google Scholar
  62. Parish A, De Waal FB (2000) The other “closest living relative”. How bonobos (Pan paniscus) challenge traditional assumptions about females, dominance, intra- and intersexual interactions, and hominid evolution. Ann N Y Acad Sci 907:97–113CrossRefGoogle Scholar
  63. Pontzer H, Wrangham RW (2006) Ontogeny of ranging in wild chimpanzees. Int J Primatol 27:295–309CrossRefGoogle Scholar
  64. Pruetz J, Bertolani P (2009) Chimpanzee (Pan troglodytes verus) behavioral responses to stresses associated with living in a savannah-mosaic environment: implications for hominin adaptations to open habitats. PaleoAnthropology 2009:252–262CrossRefGoogle Scholar
  65. Ramos-Fernández G (2005) Vocal communication in a fission–fusion society: do spider monkeys stay in touch with close associates? Int J Primatol 26:1077–1092CrossRefGoogle Scholar
  66. Riedel J, Franz M, Boesch C (2011) How feeding competition determines female chimpanzee gregariousness and ranging in the Tai National Park, Cote d’Ivoire. Am J Primatol 73:305–313CrossRefGoogle Scholar
  67. Rodrigues MA (2017) Female spider monkeys (Ateles geoffroyi) cope with anthropogenic disturbance through fission–fusion dynamics. Int J Primatol 38:838–855CrossRefGoogle Scholar
  68. Sannen A, Heistermann M, Van Elsacker L, Eens M (2003) Urinary testosterone metabolite levels within bonobos: a comparison with chimpanzees in relation to social system. Behaviour 140:683–696CrossRefGoogle Scholar
  69. Schaffner CM, Rebecchini L, Ramos-Fernandez G, Vick LG, Aureli F (2012) Spider monkeys (Ateles geoffroyi yucatenensis) cope with the negative consequences of hurricanes through changes in diet, activity budget, and fission–fusion dynamics. Int J Primatol 33:922–936CrossRefGoogle Scholar
  70. Schel AM, Rawlings B, Claidiere N, Wilke C, Wathan J, Richardson J, Pearson S, Herrelko EL S, Whiten A, Slocombe K (2013) Network analysis of social changes in a captive chimpanzee community following the successful integration of two adult groups. Am J Primatol 75:254–266CrossRefGoogle Scholar
  71. Schnell GD, Watt DJ, Douglas ME. 1985. Statistical analysis of proximity matrices: applications in animal behaviour. AnimBehav:239–253Google Scholar
  72. Seyfarth RM (1977) A model of social grooming among female primates. J Theor Biol 65:671–698CrossRefGoogle Scholar
  73. Stanford CB (1998) The social behavior of chimpanzees and bonobos. Curr Anthropol 39:399–420CrossRefGoogle Scholar
  74. Stevens JMG, Vervaecke H, De Vries H, Van Elsacker L (2006) Social structures in Pan paniscus: testing the female bonding hypothesis. Primates 47:210–217CrossRefGoogle Scholar
  75. Stumpf R (2007) Chimpanzees and bonobos: Diversity within and between species. In: Panger M, Bearder S (eds) Campbell C, Fuentes A, C M. Oxford University Press, Primates in Perspective. OxfordGoogle Scholar
  76. Sueur C, Jacobs A, Amblard F, Petit O, King AJ (2011) How can social network analysis improve the study of primate behavior? Am J Primatol 73:703–719CrossRefGoogle Scholar
  77. Surbeck M, Girard-Buttoz C, Boesch C, Crockford C, Fruth B, Hohmann G, Langergraber KE, Zuberbühler K, Wittig RM, Mundry R (2017) Sex-specific association patterns in bonobos and chimpanzees reflect species differences in cooperation. R Soc Open Sci 4:161081CrossRefGoogle Scholar
  78. Symington M (1990) Fission–fusion social organization in Ateles and Pan. Int J Primatol 11:47–61CrossRefGoogle Scholar
  79. Tokuyama N, Furuichi T (2016) Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba. Anim Behav 119:27–35CrossRefGoogle Scholar
  80. Vervaecke H, De Vries H, Van Elsacker L (2000) The pivotal role of rank in grooming and support behavior in a captive group of bonobos (Pan paniscus). Behaviour 137:1463–1485CrossRefGoogle Scholar
  81. Voelkl B, Kasper C, Schwab C (2011) Network measures for dyadic interactions: stability and reliability. Am J Primatol 73:731–740CrossRefGoogle Scholar
  82. Wakefield ML (2008) Grouping patterns and competition among female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. Int J Primatol 29:907–929CrossRefGoogle Scholar
  83. Wakefield ML (2013) Social dynamics among females and their influence on social structure in an East African chimpanzee community. Anim Behav 85:1303–1313CrossRefGoogle Scholar
  84. Walz J (2008) Male-female interaction among captive chimpanzees (Pan troglodytes) and bonobos (Pan paniscus): Who initiates? [Master’s Thesis]. The Ohio State University, ColumbusGoogle Scholar
  85. Wey T, Blumstein DT, Shen W, Jordán F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344CrossRefGoogle Scholar
  86. White FJ (1996) Comparative socio-ecology of Pan paniscus. In: McGrew W, Marchant L, Nishida T (eds) Great Ape Societies. Cambridge University Press, Cambridge, pp 29–42CrossRefGoogle Scholar
  87. White FJ (1998) Seasonality and socioecology: the importance of variation in fruit abundance to bonobo sociality. Int J Primatol 19:1013–1028CrossRefGoogle Scholar
  88. White F, Wrangham R (1988) Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour 105:148–164CrossRefGoogle Scholar
  89. Whitehead H (2009) SOCPROG programs: analyzing animal social structures. Behav Ecol Sociobiol 63:765–778CrossRefGoogle Scholar
  90. Wobber V, Wrangham R, Hare B (2010) Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees. Curr Biol 20:226–230CrossRefGoogle Scholar
  91. Wrangham R (1980) An ecological model of female-bonded primates. Behaviour 75:262–300CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Beckman Institute for Science and TechnologyUniversity of IllinoisUrbanaUSA
  2. 2.Department of PsychologyFlorida International UniversityMiamiUSA

Personalised recommendations