Abstract
Bonobos (Pan paniscus) are characterized by the formation of male-philopatric groups, wherein nulliparous females typically transfer from their natal group to another. This chapter presents long-term demographic data, collected through simultaneous observations of multiple bonobo groups at Wamba, in order to investigate the timings and locations of individual female migrations. The temporal flow from leaving the natal group, to joining a new group, and eventually to the first parturition, is documented by the retrospective classification of identified emigration and immigration events into temporary and permanent. The data presented herein update our understanding of the natal transfer process in female bonobos, which can be segmented into four phases: pre-dispersal (preparatory phase for dispersal), dispersal (practical phase for the eventual act of leaving the natal group), pre-settlement (movement phase for seeking the group in which to settle), and settlement (integration phase for becoming a fixed member of the new group). Nonetheless, further research is necessary before drawing general conclusions, as the relevant data involve only a small sample size at Wamba and other field sites are even less represented.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abondano LA, Ziegler TE, Di Fiore A (2021) Reproductive endocrinology of wild female woolly monkeys (Lagothrix lagotricha poeppigii) during puberty, ovarian cyclicity, and pregnancy. Am J Primatol 84:e23303. https://doi.org/10.1002/ajp.23303
Arandjelovic M, Head J, Boesch C, Robbins MM, Vigilant L (2014) Genetic inference of group dynamics and female kin structure in a western lowland gorilla population (Gorilla gorilla gorilla). Primate Biol 1:29–38. https://doi.org/10.5194/pb-1-29-2014
Boesch C, Boesch-Achermann H (2000) The chimpanzee of the Taï Forest: behavioural ecology and evolution. Oxford University Press, New York
Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, (15 authors), Travis JMJ (2012) Costs of dispersal. Biol Rev 87(2):290–312. https://doi.org/10.1111/j.1469-185X.2011.00201.x
Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies; relating individual behavior to spatial dynamics. Biol Rev 80:205–225. https://doi.org/10.1017/S1464793104006645
Bradley BJ, Doran-Sheehy DM, Vigilant L (2007) Potential for female kin associations in wild western gorillas despite female dispersal. Proc R Soc B Biol Sci 274:2179–2185. https://doi.org/10.1098/rspb.2007.0407
Bronson FH, Rissman EF (1986) The biology of puberty. Biol Rev 61:157–195. https://doi.org/10.1111/j.1469-185X.1986.tb00465.x
Cheng L, Samuni L, Lucchesi S, Deschner T, Surbeck M (2022a) Love thy neighbour: behavioural and endocrine correlates of male strategies during intergroup encounters in bonobos. Anim Behav 187:319–330. https://doi.org/10.1016/j.anbehav.2022.02.014
Cheng L, Shaw A, Surbeck M (2022b) Mothers stick together: how the death of an infant affects female social relationships in a group of wild bonobos (Pan paniscus). Primates 63:343–353. https://doi.org/10.1007/s10329-022-00986-2
Clutton-Brock TH (1989) Female transfer and inbreeding avoidance in social mammals. Nature 337:70–72. https://doi.org/10.1038/337070a0
Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492. https://doi.org/10.1111/j.1365-294X.2011.05232.x
Colvin JD (1986) Proximate causes of male emigration at puberty in rhesus monkeys. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior, and biology. State University of New York Press, Albany, pp 131–157
Corley M, Valeggia C, Fernandez-Duque E (2017) Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina. Horm Behav 96:42–51. https://doi.org/10.1016/j.yhbeh.2017.08.005
Douglas PH (2014) Female sociality during the daytime birth of a wild bonobo at Luikotale, Democratic Republic of the Congo. Primates 55:533–542. https://doi.org/10.1007/s10329-014-0436-0
Emery Thompson M, Newton-Fisher NE, Reynolds V (2006) Probable community transfer of parous adult female chimpanzees in the Budongo forest, Uganda. Int J Primatol 27:1601–1617. https://doi.org/10.1007/s10764-006-9098-0
Foerster S, McLellan K, Schroepfer-Walker K, Murray CM, Krupenye C, Gilby IC, Pusey AE (2015) Social bonds in the dispersing sex: partner preferences among adult female chimpanzees. Anim Behav 105:139–152. https://doi.org/10.1016/j.anbehav.2015.04.012
Forbes EE, Dahl RE (2010) Pubertal development and behavior: hormonal activation of social and motivational tendencies. Brain Cogn 72:66–72. https://doi.org/10.1016/j.bandc.2009.10.007
Furuichi T (1989) Social interactions and the life history of female Pan paniscus in Wamba, Zaire. Int J Primatol 10:173–197. https://doi.org/10.1007/BF02735199
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
Furuichi T, Yamagiwa J, Aureli F (2015) Dispersing primate females: life history and social strategies in male-philopatric species. Springer, Tokyo
Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D (1999) 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. https://doi.org/10.1098/rspb.1999.0762
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge, MA
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. https://doi.org/10.1016/S0003-3472(80)80103-5
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
Heistermann M, Möhle U, Vervaecke H, van Elsacker L, Keith Hodges J (1996) Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biol Reprod 55:844–853. https://doi.org/10.1095/biolreprod55.4.844
Hohmann G (2001) Association and social interactions between strangers and residents in bonobos (Pan paniscus). Primates 42:91–99. https://doi.org/10.1007/BF02640692
Idani G (1990) Relationships between unit-groups of bonobos at Wamba, Zaire: encounters and temporary fusions. Afr Study Monogr 11:153–186. https://doi.org/10.14989/68066
Idani G (1991) Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatol 57:83–95. https://doi.org/10.1159/000156568
Isbell LA, Van Vuren D (1996) Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133:1–36. https://doi.org/10.1163/156853996X00017
Ishizuka S, Toda K, Furuichi T (2019) Genetic analysis of migration pattern of female bonobos (Pan paniscus) among three neighboring groups. Int J Primatol 41:401–414. https://doi.org/10.1007/s10764-019-00106-w
Kahlenberg SM, Thompson ME, Muller MN, Wrangham RW (2008) Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Anim Behav 76:1497–1509. https://doi.org/10.1016/j.anbehav.2008.05.029
Kano T (1992) The last ape: pygmy chimpanzee behavior and ecology. Stanford University Press, Stanford, CA
Kawazoe T, Sosa S (2019) Social networks predict immigration success in wild Japanese macaques. Primates 60(3):213–222. https://doi.org/10.1007/s10329-018-0702-7
Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS One 11:e0154845. https://doi.org/10.1371/journal.pone.0154845
Kuroda S (1979) Grouping of the pygmy chimpanzees. Primates 20:161–183. https://doi.org/10.1007/BF02373371
Kuroda S (1989) Developmental retardation and behavioral characteristics of pygmy chimpanzees. In: Heltne PG, Marquardt LA (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 184–193
Langergraber K, Mitani J, Vigilant L (2009) Kinship and social bonds in female chimpanzees (Pan troglodytes). Am J Primatol 71:840–851. https://doi.org/10.1002/ajp.20711
Lathouwers MD, Elsacker LV (2005) Reproductive parameters of female Pan paniscus and P. troglodytes: quality versus quantity. Int J Primatol 26:55–71. https://doi.org/10.1007/s10764-005-0723-0
Lee PC, Strier KB (2015) Complexities of understanding female dispersal in primates. In: Furuichi T, Yamagiwa J, Aureli F (eds) Dispersing primate females: life history and social strategies in male-philopatric species. Springer, Tokyo, pp 215–230
Lee SM, Murray CM, Lonsdorf EV, Fruth B, Stanton MA, Nichols J, Hohmann G (2020) Wild bonobo and chimpanzee females exhibit broadly similar patterns of behavioral maturation but some evidence for divergence. Am J Phys Anthropol 171:100–109. https://doi.org/10.1002/ajpa.23935
Lehmann J, Boesch C (2009) Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. Anim Behav 77:377–387. https://doi.org/10.1016/j.anbehav.2008.09.038
Lemoine S, Crockford C, Wittig RM (2019) Spatial integration of unusually high numbers of immigrant females into the south group: further support for the bisexually-bonded model in Taï chimpanzees. In: Boesch C, Wittig RM, Crockford C, Vigilant L, Deschner T, Leendertz F (eds) The chimpanzees of the Taï forest: 40 years of research. Cambridge University Press, Cambridge, pp 159–177
Lemoine SRT, Samuni L, Crockford C, Wittig RM (2022) Parochial cooperation in wild chimpanzees: a model to explain the evolution of parochial altruism. Philos Trans R Soc B Biol Sci 377:20210149. https://doi.org/10.1098/rstb.2021.0149
Lucchesi S, Cheng L, Janmaat K, Mundry R, Pisor A, Surbeck M (2020) Beyond the group: how food, mates, and group size influence intergroup encounters in wild bonobos. Behav Ecol 31(2):519–532. https://doi.org/10.1093/beheco/arz214
Manguette ML, Robbins AM, Breuer T, Stokes EJ, Parnell RJ, Robbins MM (2019) Intersexual conflict influences female reproductive success in a female-dispersing primate. Behav Ecol Sociobiol 73:118. https://doi.org/10.1007/s00265-019-2727-3
Manguette ML, Robbins AM, Breuer T, Stokes EJ, Parnell RJ, Robbins MM (2020) Female dispersal patterns influenced by male tenure duration and group size in western lowland gorillas. Behav Ecol Sociobiol 74:81. https://doi.org/10.1007/s00265-020-02863-8
Markham AC, Lonsdorf EV, Pusey AE, Murray CM (2015) Maternal rank influences the outcome of aggressive interactions between immature chimpanzees. Anim Behav 100:192–198. https://doi.org/10.1016/j.anbehav.2014.12.003
Matsumoto T, Hanamura S, Kooriyama T, Hayakawa T, Inoue E (2021) Female chimpanzees giving first birth in their natal group in Mahale: attention to incest between brothers and sisters. Primates 62:279–287. https://doi.org/10.1007/s10329-020-00886-3
Mitchell CL (1994) Migration alliances and coalitions among adult male South American squirrel monkeys (Saimiri sciureus). Behaviour 130:169–190. https://doi.org/10.1163/156853994X00514
Moore J (1984) Female transfer in primates. Int J Primatol 5:537–589. https://doi.org/10.1007/BF02692285
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 163:158–172. https://doi.org/10.1002/ajpa.23197
Mulavwa M, Furuichi T, Yangozene K, Yamba-Yamba M, Motema-Salo B, 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, and conservation. Springer, New York, pp 121–134
Nicolson N (1987) Infants, mothers and other females. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 330–342
Nishida T (1989) Social interactions between resident and immigrant female chimpanzees. In: Heltne PG, Marquardt L (eds) Understanding chimpanzees. Cambridge University Press, Cambridge, pp 68–89
Nishida T, Hiraiwa-Hasegawa M, Hasegawa T, Takahata Y (1985) Group extinction and female transfer in wild chimpanzees in the Mahale National Park, Tanzania. Z Tierpsychol 67:284–301. https://doi.org/10.1111/j.1439-0310.1985.tb01395.x
Parish AR (1994) Sex and food control in the “uncommon chimpanzee”: how bonobo females overcome a phylogenetic legacy of male dominance. Ethol Sociobiol 15:157–179. https://doi.org/10.1016/0162-3095(94)90038-8
Pusey AE (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 115:203–246. https://doi.org/10.1163/156853990X00581
Pusey AE, Packer C (1987) Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 250–266
Pusey AE, Schroepfer-Walker K (2013) Female competition in chimpanzees. Philos Trans R Soc B Biol Sci 368:20130077. https://doi.org/10.1098/rstb.2013.0077
Pusey AE, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206. https://doi.org/10.1016/0169-5347(96)10028-8
Robbins AM, Stoinski TS, Fawcett KA, Robbins MM (2009) Does dispersal cause reproductive delays in female mountain gorillas? Behavior 146:525–549. https://doi.org/10.1163/156853909X426354
Rudicell RS, Jones JH, Wroblewski EE, Learn GH, Li Y, Robertson JD, Greengrass E, Grossmann F, (11 authors), Wilson ML (2010) Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog 6(9):e1001116. https://doi.org/10.1371/journal.ppat.1001116
Sakamaki T, Nakamura M (2015) Intergroup relationships. In: Nakamura M, Hosaka K, Itoh N, Zamma K (eds) Mahale chimpanzees: 50 years of research. Cambridge University Press, Cambridge, pp 128–140
Sakamaki T, Tokuyama N (2023) Potential benefits of intergroup associations and chronological changes of intergroup relationships in bonobos. In: Furuichi T, Idani G, Kimura D, Ihobe H, Hashimoto C (eds) Bonobos and people at Wamba: 50 years of research. Springer, Singapore, pp 311-332
Sakamaki T, Behncke I, Laporte M, Mulavwa M, Ryu H, Takemoto H, Tokuyama N, Yamamoto S, Furuichi T (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. Springer, Tokyo, pp 127–164
Sakamaki T, Ryu H, Toda K, Tokuyama N, Furuichi T (2018) Increased frequency of intergroup encounters in wild bonobos (Pan paniscus) around the yearly peak in fruit abundance at Wamba. Int J Primatol 39:685–704. https://doi.org/10.1007/s10764-018-0058-2
Schoof VAM, Jack KM, Isbell LA (2009) What traits prompt male parallel dispersal in primates? Behaviour 146:701–726. https://doi.org/10.1163/156853908X399086
Strier KB, Ziegler TE (2000) Lack of pubertal influences on female dispersal in muriqui monkeys, Brachyteles arachnoides. Anim Behav 59:849–860. https://doi.org/10.1006/anbe.1999.1387
Strier KB, Possamai CB, Mendes SL (2015) Dispersal patterns of female northern muriquis; implications for social dynamics, life history, and conservation. In: Furuichi T, Yamagiwa J, Aureli F (eds) Dispersing primate females: life history and social strategies in male-philopatric species. Springer, Tokyo, pp 3–22
Stumpf RM, Thompson ME, Muller MN, Wrangham RW (2009) The context of female dispersal in Kanyawara chimpanzees. Behaviour 146:629–656. https://doi.org/10.1163/156853909X413853
Sugiyama Y, Fujita S (2011) The demography and reproductive parameters of Bossou chimpanzees. In: Matsuzawa T, Humle T, Sugiyama Y (eds) The chimpanzees of Bossou and Nimba. Springer, Tokyo, pp 23–34
Surbeck M, Hohmann G (2013) Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus). Behav Ecol Sociobiol 67:1767–1780. https://doi.org/10.1007/s00265-013-1584-8
Takahata Y (2015) Disappearance of K-group male chimpanzees: re-examination of group extinction. In: Nakamura M, Hosaka K, Itoh N, Zamma K (eds) Mahale chimpanzees: 50 years of research. Cambridge University Press, Cambridge, pp 119–127
Thompson-Handler N, Malenky RK, Reinartz GE (1995) Action plan for Pan paniscus: report on free ranging populations and proposals for their preservation. Zoological Society of Milwaukee County, Milwaukee
Toda K, Furuichi T (2020) Low resistance of senior resident females toward female immigration in bonobos (Pan paniscus) at Wamba, Democratic Republic of the Congo. Int J Primatol 41:415–427. https://doi.org/10.1007/s10764-019-00126-6
Toda K, Furuichi T (2022) Do immigrant female bonobos prefer older resident females as important partners when integrating into a new group? Primates 63:123–136. https://doi.org/10.1007/s10329-021-00971-1
Toda K, Tokuyama N, Ishizuka S, Furuichi T (2018) A short-term visit of an adult male bonobo from the neighboring unit-group at Wamba. Pan Afr News 25:22–24
Toda K, Ryu H, Furuichi T (2021) Age and sex differences in juvenile bonobos in party associations with their mothers at Wamba. Primates 62:19–27. https://doi.org/10.1007/s10329-020-00853-y
Toda K, Mouri K, Ryu H, Sakamaki T, Tokuyama N, Yokoyama T, Shibata S, Poiret ML, (2 authors), Furuichi T (2022) Do female bonobos (Pan paniscus) disperse at the onset of puberty? Hormonal and behavioral changes related to their dispersal timing. Horm Behav 142:105159. https://doi.org/10.1016/j.yhbeh.2022.105159
Tokuyama N, Furuichi T (2016) Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba. Anim Behav 119:27–35. https://doi.org/10.1016/j.anbehav.2016.06.021
Tokuyama N, Sakamaki T, Furuichi T (2019) Inter-group aggressive interaction patterns indicate male mate defense and female cooperation across bonobo groups at Wamba, Democratic Republic of the Congo. Am J Phys Anthropol 170:535–550. https://doi.org/10.1002/ajpa.23929
Tokuyama N, Toda K, Poiret ML, Iyokango B, Bakaa B, Ishizuka S (2021) Two wild female bonobos adopted infants from a different social group at Wamba. Sci Rep 11:4967. https://doi.org/10.1038/s41598-021-83667-2
Walker KK, Pusey AE (2020) Inbreeding risk and maternal support have opposite effects on female chimpanzee dispersal. Curr Biol 30(2):R62–R63. https://doi.org/10.1016/j.cub.2019.11.081
Walker KK, Walker CS, Goodall J, Pusey AE (2018) Maturation is prolonged and variable in female chimpanzees. J Hum Evol 114:131–140. https://doi.org/10.1016/j.jhevol.2017.10.010
White FJ (1988) Party composition and dynamics in Pan paniscus. Int J Primatol 9:179–193. https://doi.org/10.1007/BF02737400
White FJ (1996) Pan paniscus 1973 to 1996: twenty-three years of field research. Evol Anthropol 5:11–17. https://doi.org/10.1002/(SICI)1520-6505(1996)5:1<11::AID-EVAN5>3.0.CO;2-Z
Wikberg EC, Sicotte P, Campos FA, Ting N (2012) Between-group variation in female dispersal, kin composition of groups, and proximity patterns in a black-and-white colobus monkey (Colobus vellerosus). PLoS One 7(11):e48740. https://doi.org/10.1371/journal.pone.0048740
Wikberg EC, Jack KM, Campos FA, Fedigan LM, Sato A, Bergstrom ML, Hiwatashi T, Kawamura S (2014) The effect of male parallel dispersal on the kin composition of groups in white-faced capuchins. Anim Behav 96:9–17. https://doi.org/10.1016/j.anbehav.2014.07.016
Wittig RM, Boesch C (2019) Demography and life history of five chimpanzee communities in Taï National Park. In: Boesch C, Wittig R, Crockford C, Vigilant L, Deschner T, Leendertz F (eds) The chimpanzees of the Taï forest: 40 years of research. Cambridge University Press, Cambridge, pp 125–140
Acknowledgments
We are deeply grateful to Drs. T. Furuichi, G. Idani, H. Ihobe, and C. Hashimoto for giving us the opportunity to present our work. Demographic data presented in this chapter have been collected with the help of many researchers who have worked at this field site, specifically Dr. T. Furuichi, Dr. M. N. Mulavwa, Dr. H. Ryu, Dr. K. E. Graham, Dr. H. Takemoto, Dr. S. Ishizuka, Dr. T. Yokoyama, Dr. S. Shibata, Ms. M. Poiret, and Mr. J. B. Bakaa. The fieldwork of K. Toda was financially supported by the Leading Program in Primatology and Wildlife Science of Kyoto University (coordinated by Dr. T. Matsuzawa), Grant-in-Aid for Scientific Research [17J01336] by the Japanese Society for the Promotion of Science, Young Explorers Grant from the National Geographic Foundation for Science and Exploration [Asia 38-16], and Canon Foundation in Europe–Kyoto University Japan–Africa Exchange Fellowship
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Toda, K., Tokuyama, N., Sakamaki, T. (2023). Multiple Phases of Natal Transfer Process in Female Bonobos and Factors Underlying Each Phase: Findings from Long-Term Observations in Wild Populations. In: Furuichi, T., Idani, G., Kimura, D., Ihobe, H., Hashimoto, C. (eds) Bonobos and People at Wamba: 50 Years of Research. Springer, Singapore. https://doi.org/10.1007/978-981-99-4788-1_15
Download citation
DOI: https://doi.org/10.1007/978-981-99-4788-1_15
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-99-4787-4
Online ISBN: 978-981-99-4788-1
eBook Packages: Social SciencesSocial Sciences (R0)