Skip to main content

Intergroup Transfer of Females and Social Relationships Between Immigrants and Residents in Bonobo (Pan paniscus) Societies

  • Chapter
Dispersing Primate Females

Abstract

This paper first reviews data collected from 1976 to 2013 regarding the life histories of members of the main E1 study group of bonobos (Pan paniscus) in Wamba. The E1 group exhibited strong tendencies toward female dispersal and male residence during the entire study period, thereby exemplifying the typical characteristics of a male-philopatric and female-dispersal society. This pattern did not change after the abandonment of artificial provisioning. We then present two new cases of immigrant females, focusing especially on social association patterns, dominance relationships, and affiliative interactions during the approximate 2.5 years from the time of their immigration to their first birth. These females began engaging in social grooming with resident females immediately after their arrival but rarely did so with adult males, suggesting that they regard social bonding with females as more important than that with males. They also emigrated at a young age and frequently engaged in social play. Indeed, social bonding established through frequent social play may be related to the development of socially symmetrical relationships, which are the basis for the egalitarian bonobo society. Intragroup competition for food and mates was unlikely explanations for the tendency toward female dispersal. However, male residence and the risk of father–daughter incest may encourage female transfer among bonobos.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J, Chapman CA, Connor R, Di Fiore A, Dunbar RIM, Henzi SP, Holekamp K, Korstjens AH, Layton R, Lee P, Lehmann J, Manson JH, Ramos-Fernandez G, Strier KB, van Schaik CP (2008) Fission–fusion dynamics: new research frameworks. Curr Anthropol 49:627–654

    Article  Google Scholar 

  • Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201:163–165

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH (1989) Female transfer and inbreeding avoidance in mammals. Nature 337:70–71

    Article  CAS  PubMed  Google Scholar 

  • de Waal FBM (1982) Chimpanzee politics: power and sex among apes. Harper & Row, New York

    Google Scholar 

  • de Waal FBM (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106:183–251

    Article  Google Scholar 

  • Dobson FS (1982) Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 30:1183–1192

    Article  Google Scholar 

  • Emery Thompson M (2013) Reproductive ecology of female chimpanzees. Am J Primatol 75:222–237

    Article  Google Scholar 

  • Enomoto T (1990) Social play and sexual behavior of the bonobo (Pan paniscus) with special reference to flexibility. Primates 31:469–480

    Article  Google Scholar 

  • Fagen R (1981) Animal play behavior. Oxford University Press, New York

    Google Scholar 

  • Furuichi T (1987) Sexual swelling, receptivity, and grouping of wild pygmy chimpanzee female at Wamba, Zaire. Primates 28:309–318

    Article  Google Scholar 

  • Furuichi T (1989) Social interactions and the life history of female Pan paniscus in Wamba, Zaïre. Int J Primatol 10:173–197

    Article  Google Scholar 

  • Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba, Zaire. Int J Primatol 18:855–875

    Article  Google Scholar 

  • Furuichi T (2011) Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20:131–142

    Article  PubMed  Google Scholar 

  • Furuichi T, Ihobe H (1994) Variation in male relationships in bonobos and chimpanzees. Behaviour 130:211–228

    Article  Google Scholar 

  • Furuichi T, Hashimoto C, Idani G, Ihobe H, Tashiro Y, Kano T (1999) Current situation of studies of bonobos (Pan paniscus) at Wamba, D. R. Congo. Primate Res 15:115–127 (in Japanese with English summary)

    Article  Google Scholar 

  • Furuichi T, Idani G, Ihobe H, Hashimoto C, Tashiro Y, Sakamaki T, Mulavwa MN, Yangozene K, Kuroda S (2012) Long-term studies on wild bonobos at Wamba, Luo Scientific Reserve, D. R. Congo: towards the understanding of female life history in a male-philopatric species. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 413–433

    Chapter  Google Scholar 

  • Genty E, Clay Z, Hobaiter C, Zuberbühler K (2014) Multi-modal use of a socially directed call in bonobos. PLoS ONE 9(1):e84738. doi:10.1371/journal.pone.0084738

    Article  PubMed Central  PubMed  Google Scholar 

  • Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D (2011) Intracommunity relationships, dispersal pattern and paternity success in a wild living community of bonobos (Pan paniscus) determined from DNA analysis of faecal samples. Proc R Soc B Biol Sci 266:1189–1195

    Article  Google Scholar 

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Greenwood PJ (1980) Mating system, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488

    Article  CAS  PubMed  Google Scholar 

  • Handley LJL, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578

    Article  Google Scholar 

  • Hashimoto C (1997) Context and development of sexual behavior of wild bonobos (Pan paniscus) at Wamba, Zaire. Int J Primatol 18:1–21

    Article  Google Scholar 

  • Hashimoto C, Furuichi T (2001) Intergroup transfer and inbreeding avoidance in bonobos. Primate Res 17:259–269 (in Japanese with English summary)

    Article  Google Scholar 

  • Hashimoto C, Furuichi T, Takenaka O (1996) Matrilineal kin relationship and social behavior of wild bonobos (Pan paniscus): sequencing the D-loop region of mitochondrial DNA. Primates 37:305–318

    Article  Google Scholar 

  • Hashimoto C, Tashiro Y, Hibino E, Mulavwa M, Yangozene K, Furuichi T, Idani G, Takenaka O (2008) Longitudinal structure of a unit-group of bonobos: male philopatry and possible fusion of unit-groups. In: Furuichi T, Thompson J (eds) The bonobos: behavior, ecology, and conservation. Springer, New York, pp 107–119

    Chapter  Google Scholar 

  • Hayaki H (1985) Social play of juvenile and adolescent chimpanzees in the Mahale Mountains National Park, Tanzania. Primates 26:343–360

    Article  Google Scholar 

  • Hohmann G (2001) Association and social interactions between strangers and residents in bonobos (Pan paniscus). Primates 42:91–99

    Article  Google Scholar 

  • Hohmann G, Fruth B (2000) Use and function of genital contacts among female bonobos. Anim Behav 60:107–120

    Article  PubMed  Google Scholar 

  • Idani G (1990) Relations between unit-groups of bonobos at Wamba, Zaire: encounters and temporary fusions. Afr Study Monogr 11:153–186

    Google Scholar 

  • Idani G (1991) Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatol 57:83–95

    Article  CAS  PubMed  Google Scholar 

  • Idani G, Mwanza N, Ihobe H, Hashimoto C, Tashiro Y, Furuichi T (2008) Changes in the status of bonobos, their habitat, and the situation of humans at Wamba in the Luo Scientific Reserve, Democratic Republic of Congo. In: Furuichi T, Thompson J (eds) The bonobos: behavior, ecology, and conservation. Springer, New York, pp 291–302

    Chapter  Google Scholar 

  • Itani J (1972) A preliminary essay on the relationship between social organization and incest avoidance in nonhuman primates. In: Poirier FR (ed) Primate socialization. Random House, New York, pp 165–171

    Google Scholar 

  • Itani J (1977) Evolution of primate social structure. J Hum Evol 6:235–243

    Article  Google Scholar 

  • Itani J (1985) The evolution of primate social structures. Man 20:593–611

    Article  Google Scholar 

  • Kahlenberg SM, Emery Thompson M, Wrangham RW (2008a) Female competition over core areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda. Int J Primatol 29:931–947

    Article  Google Scholar 

  • Kahlenberg SM, Emery Thompson M, Muller MN, Wrangham RW (2008b) Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Anim Behav 76:1497–1509

    Article  Google Scholar 

  • Kano T (1982) The social group of pygmy chimpanzees (Pan paniscus) of Wamba. Primates 23:171–188

    Article  Google Scholar 

  • Kano T (1992) The last ape: pigmy chimpanzee behavior and ecology. Stanford University Press, Stanford

    Google Scholar 

  • Kuroda S (1979) Grouping of the pygmy chimpanzees. Primates 20:161–183

    Article  Google Scholar 

  • Kuroda S (1980) Social behavior of the pygmy chimpanzees. Primates 21:181–197

    Article  Google Scholar 

  • Kuroda S (1989) Developmental retardation and behavioral characteristics. In: Heltne PG, Marquardt LA (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 184–193

    Google Scholar 

  • Le Galliard J-F, Gundersen G, Andreassen HP, Stenseth NC (2006) Natal dispersal, interactions among siblings and intrasexual competition. Behav Ecol 17:733–740

    Article  Google Scholar 

  • Moore J, Ali R (1984) Are dispersal and inbreeding avoidance related? Anim Behav 32:94–112

    Article  Google Scholar 

  • Nishida T (1979) The social structure of chimpanzees of the Mahale Mountains. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings Publishing, Menlo Park, pp 73–121

    Google Scholar 

  • Nishida T (1989) Social interactions between resident and immigrant female chimpanzees. In: Heltne PG, Marquardt L (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 68–89

    Google Scholar 

  • Nishida T (2012) Chimpanzees of the Lakeshore: natural history and culture at Mahale. Cambridge University Press, Cambridge

    Google Scholar 

  • Nishida T, Hiraiwa-Hasegawa M (1987) Chimpanzees and bonobos: cooperative relationships among males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 165–177

    Google Scholar 

  • Nishida T, Kano T, Goodall J, McGrew WC, Nakamura M (1999) Ethogram and ethnography of Mahale chimpanzees. Anthropol Sci 107:141–188

    Article  Google Scholar 

  • Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59:99–121

    Article  PubMed  Google Scholar 

  • 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 129:418–426

    Article  PubMed  Google Scholar 

  • Perrin N, Lehmann L (2001) Is sociality driven by the costs of dispersal or the benefits of philopatry? A role for kin-discrimination mechanisms. Am Nat 158:471–483

    Article  CAS  PubMed  Google Scholar 

  • Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299

    Article  CAS  PubMed  Google Scholar 

  • Pusey A, Murray C, Wallauer W, Wilson M, Wroblewski E, Goodall J (2008) Severe aggression among female Pan troglodytes schweinfurthii at Gombe National Park, Tanzania. Int J Primatol 29:949–973

    Article  Google Scholar 

  • Ryu H, Hill DA, Furuichi T (2014) Prolonged maximal sexual swelling in wild bonobos facilitates affiliative interactions between females. Behaviour. doi:10.1163/1568539X-00003212

    Google Scholar 

  • Sakamaki T (2013) Social grooming among wild bonobos (Pan paniscus) at Wamba in the Luo Scientific Reserve, DR Congo, with special reference to the formation of grooming gatherings. Primates 54:349–359

    Article  PubMed  Google Scholar 

  • Sakamaki T, Mulavwa M, Furuichi T (2009) Flu-like epidemics in wild bonobos (Pan paniscus) at Wamba, the Luo Scientific Reserve, Democratic Republic of Congo. Pan Afr News 16:1–4

    Google Scholar 

  • Shea BT (1983) Paedomorphosis and neoteny in the pygmy chimpanzee. Science 222:521–522

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama Y (1999) Socioecological factors of male chimpanzee migration at Bossou, Guinea. Primates 40:61–68

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama Y (2004) Demographic parameters and life history of chimpanzees at Bossou, Guinea. Am J Phys Anthropol 124:154–165

    Article  PubMed  Google Scholar 

  • Surbeck M, Mundry R, Hohmann G (2011) Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc R Soc B 278:590–598

    Article  PubMed Central  PubMed  Google Scholar 

  • Tashiro Y, Idani G, Kimura D, Bongori L (2007) Habitat changes and decreases in the bonobo population in Wamba, Democratic Republic of the Congo. Afr Study Monogr 28:99–106

    Google Scholar 

  • Thompson-Handler N, Malenky RK, Badrian N (1984) Sexual behavior of Pan paniscus under natural conditions in the Lomako Forest, Equateur, Zaire. In: Susman RL (ed) The pygmy chimpanzee: its evolutionary biology and behavior. Plenum Press, New York, pp 347–368

    Chapter  Google Scholar 

  • Waser PM (1985) Does competition drive dispersal? Ecology 66:1170–1175

    Article  Google Scholar 

  • White FJ (1988) Party composition and dynamics in Pan paniscus. Int J Primatol 9:179–193

    Article  Google Scholar 

  • White FJ (1996) Pan paniscus 1973 to 1996: twenty-three years of field research. Evolut Anthropol 5:11–17

    Article  Google Scholar 

  • White FJ, Wood KD (2007) Female feeding priority in bonobos, Pan paniscus, and the question of female dominance. Am J Primatol 69:837–850

    Article  PubMed  Google Scholar 

  • Wrangham RW (1986) Ecology and social relationships in two species of chimpanzees. In: Rubenstein DL, Wrangham RW (eds) Ecological aspect of social evolution. Princeton University Press, Princeton, pp 352–378

    Google Scholar 

Download references

Acknowledgments

This study was financially supported by the Japan Ministry of the Environment Global Environment Research Fund (F-061 to Nishida; D-1007 to Furuichi), Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (21255006 to Ihobe; 22255007 to Furuichi), JSPS Asia–Africa Science Platform Program (2009–2011, 2012–2014 to Furuichi), JSPS HOPE project of the Primate Research Institute (PRI) of Kyoto University (to Matsuzawa), US Fish and Wildlife Service Assistance Award (96200-0-G017 to the African Wildlife Foundation), Ministry of Education, Culture, Sports, Science & Technology in Japan special grant (“Human Evolution”), and JSPS Grants-in-Aid for Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation (to PRI, Kyoto University). We thank Mr. I. Monkengo and Dr. N. Mwanza of the Research Center for Ecology and Forestry; Mr. F. Bukasa of the Ministry of Scientific Research and Technology in the DRC for research permits and logistical support; Mrs. B. Luunga, B. Bokamba, I. Bafanande, B. Likombe, N. Isoluka, E. Besao, and other workers and villagers at Wamba for collecting data and cooperating with our study; members of the Department of Biology of Meiji Gakuin University and PRI of Kyoto University; and the late Drs. T. Nishida, T. Matsuzawa, S. Kuroda, G. Idani, H. Ihobe, D. Kimura, C. Hashimoto, Y. Tashiro, and Y. Tsuji for support and encouragement.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tetsuya Sakamaki .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Sakamaki, T. et al. (2015). Intergroup Transfer of Females and Social Relationships Between Immigrants and Residents in Bonobo (Pan paniscus) Societies. In: Furuichi, T., Yamagiwa, J., Aureli, F. (eds) Dispersing Primate Females. Primatology Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55480-6_6

Download citation

Publish with us

Policies and ethics