Non-conceptive Sexual Interactions in Monkeys, Apes, and Dolphins

  • Takeshi Furuichi
  • Richard Connor
  • Chie Hashimoto
Part of the Primatology Monographs book series (PrimMono)


Primates and dolphins exhibit comparable examples of all categories of non-conceptive sexual behaviors, including sexual interactions involving immature individuals, those involving individuals of the same sex, and copulation during the non-conceptive period. Although mammals of other taxa also perform non-conceptive sexual behaviors, the fact that there are so many reports of non-conceptive sexual interactions among higher primates and dolphins suggest a link between the nonreproductive use of sexual behaviors and high intelligence. This link might be because the greater role of learning in sexual behavior expands the possibility for sex to be incorporated into a variety of non-conceptive functions. Non-conceptive sexual behaviors seem to reflect or be influenced by important social factors, including affiliative relations and alliance between individuals of the same or different sex, high social status of females, within-group or between-group tension resolution, mate selection, and infanticide prevention. Animals may employ non-conceptive sexual behaviors to control various important aspects of their relationships with others which they cannot control with other social behaviors, which suggests that instances of non-conceptive sexual behaviors may serve as keys to understanding important aspects of the social relationships or social structure of the species.


Bonobo Bottlenose dolphin Estrus Homosexual Non-conceptive • Sexual behavior 



Studies on chimpanzees and bonobos by Furuichi and Hashimoto were mainly funded by the Japan Society for the Promotion of Science (JSPS) Grants-in-aid for Scientific Research, JSPS Core-to-Core program, JSPS International Training Program, JSPS Asia-Africa Science Platform Program, JSPS Institutional Program for Young Researcher Overseas Visits, Japan Ministry of the Environment (JME) Global Environment Research Fund, JME Environment Research and Technology Development Fund, the National Geographic Fund for Research and Exploration, and Toyota Foundation. We thank Drs. Takayoshi Kano, Toshisada Nishida, Juichi Yamagiwa, Tetsuro Matsuzawa and other members of Primate Research Institute and Laboratory of Human Evolution of Kyoto University, and Drs. Mwanza Ndunda, Mbangi Norbert Mulavwa and other stuff of Ministry of Scientific Research of D.R. Congo for their continued support for our studies. The data on dolphins analyzed by Connor were funded by an NSF Dissertation Improvement Grant and grants from The National Geographic Society and a Fulbright Fellowship to Australia.


  1. Bagemihl B (1999) Biological exuberance: animal homosexuality and natural diversity. St. Martins Press, New YorkGoogle Scholar
  2. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Tai forest: behavioural ecology and evolution. Oxford University Press, New YorkGoogle Scholar
  3. Connor RC, Smolker RA (1995) Seasonal changes in the stability of male–male bonds in Indian Ocean bottlenose dolphins (Tursiops sp.). Aquat Mamm 21:213–216Google Scholar
  4. Connor RC, Smolker RA (1996) “Pop” goes the dolphin: a vocalization male bottlenose dolphins produce during consortships. Behaviour 133:643–662CrossRefGoogle Scholar
  5. Connor RC, Volmer NL (2009) Sexual coercion in dolphin consortships: a comparison with chimpanzees. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 218–243Google Scholar
  6. Connor RC, Smolker RA, Richards AF (1992a) Two levels of alliance formation among male bottlenose dolphins (Tursiops sp.). Proc Natl Acad Sci USA 89:987–990CrossRefPubMedCentralPubMedGoogle Scholar
  7. Connor RC, Smolker RA, Richards AF (1992b) Dolphin alliances and coalitions. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in animals and humans. Oxford University Press, OxfordGoogle Scholar
  8. Connor RC, Richards AF, Smolker RA, Mann J (1996) Patterns of female attractiveness in Indian Ocean bottlenose dolphins. Behaviour 133:37–69CrossRefGoogle Scholar
  9. Connor RC, Wells R, Mann J, Read A (2000) The bottlenose dolphin: social relationships in a fission–fusion society. In: Mann J, Connor R, Tyack P, Whitehead H (eds) Cetacean societies: field studies of whales and dolphins. University of Chicago Press, Chicago, pp 91–126Google Scholar
  10. de Waal FBM (1987) Tension regulation and nonreproductive functions of sex in captive bonobos (Pan paniscus). Natl Geogr Res 3:318–335Google Scholar
  11. Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, OxfordGoogle Scholar
  12. Dunn DG, Barco SG, Pabst DA, McLellan WA (2002) Evidence for infanticide in bottlenose dolphins of the western north Atlantic. J Wildl Dis 38:505–510CrossRefPubMedGoogle Scholar
  13. Ellison PT, Panter-Brick C, Lipson SF, O’Rourke MT (1993) The ecological context of human ovarian function. Human Reproduction 8:2248–2258Google Scholar
  14. Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin. Cambridge University Press, CambridgeGoogle Scholar
  15. Fujita S, Mitsunaga F, Sugiura H, Shimizu K (2001) Measurement of urinary and fecal steroid metabolites during the ovarian cycle in captive and wild Japanese macaques, Macaca fuscata. Am J Primatol 53:167–176CrossRefPubMedGoogle Scholar
  16. Fujita G, Sugiura H, Mitsunaga F, Shimizu K (2004) Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata). Am J Primatol 64:367–375CrossRefPubMedGoogle Scholar
  17. Furuichi T (1985) Inter-male associations in a wild Japanese macaque troop on Yakushima Island, Japan. Primates 26:219–237CrossRefGoogle Scholar
  18. Furuichi T (1987) Sexual swelling receptivity and grouping of wild pygmy chimpanzee females at Wamba Zaire. Primates 28:309–318CrossRefGoogle Scholar
  19. Furuichi T (1989) Social interactions and the life history of female Pan paniscus in Wamba Zaire. Int J Primatol 10:173–197CrossRefGoogle Scholar
  20. Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 18:855–875CrossRefGoogle Scholar
  21. Furuichi T (2006) Evolution of the social structure of hominoids: reconsideration of food distribution and the estrus sex ratio. In: Ishida H, Tuttle R, Pickford M, Ogihara N, Nakatsukasa M (eds) Human origins and environmental backgrounds. Springer, New York, pp 235–248CrossRefGoogle Scholar
  22. Furuichi T (2009) Factors underlying party size differences between chimpanzees and bonobos: a review and hypotheses for future study. Primates 50:197–209CrossRefPubMedGoogle Scholar
  23. Furuichi T (2011) Female contribution to the peaceful nature of bonobo society. Evol Anthropol 20:131–142CrossRefPubMedGoogle Scholar
  24. Furuichi T, Idani G, Ihobe H, Hashimoto C, Tashiro Y, Sakamaki T, Mulavwa MN, Yangozene K, Kuroda S (2012) Long-term study on wild bonobos at Wamba, Luo Scientific Reserve, D. R. Congo: towards the understanding of female life history in a male-philopatric species. In: Kappler PM, Watts DP (eds) Long term field study of primates. Springer-Verlag, Berlin, Heidelberg, pp 413–433Google Scholar
  25. Furuichi T, Hashimoto C (2002) Why female bonobos have a lower copulation rate during estrus than chimpanzees. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 156–167CrossRefGoogle Scholar
  26. Furuichi T, Hashimoto C (2004) Sex differences in copulation attempts in wild bonobos at Wamba. Primates 45:59–62CrossRefPubMedGoogle Scholar
  27. Furuichi T, Ihobe H (1994) Variation in male relationships in bonobos and chimpanzees. Behaviour 130:211–228CrossRefGoogle Scholar
  28. Furuichi T, Idani G, Ihobe H, Kuroda S, Kitamura K, Mori A, Enomoto T, Okayasu N, Hashimoto C, Kano T (1998) Population dynamics of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 19:1029–1043CrossRefGoogle Scholar
  29. Furuichi T, Mulavwa M, Yangozene K, Yamba-Yamba M, Motema-Salo B, Idani G, Ihobe H, Hashimoto C, Tashiro Y, Mwanza N (2008) Relationships among fruit abundance, ranging rate, and party size and composition of bonobos at Wamba. In: Furuichi T, Thompson J (eds) The bonobos: behavior, ecology, and conservation. Springer, New York, pp 135–149CrossRefGoogle Scholar
  30. 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 Lond B 266:1189–1195CrossRefGoogle Scholar
  31. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, CambridgeGoogle Scholar
  32. Harcourt AH, Stewart KJ (2007) Gorilla society: conflict, compromise, and cooperation between sexes. Chicago University Press, ChicagoCrossRefGoogle Scholar
  33. Harcourt AH, Stewart KJ, Fossey D (1981) Gorilla reproduction in the wild. In: Graham CE (ed) Reproductive biology of the great apes: comparative and biomedical perspectives. Academic, New York, pp 265–279CrossRefGoogle Scholar
  34. Hasegawa T, Hiraiwa-Hasegawa M (1983) Opportunistic and restrictive mating among wild chimpanzees in the Mahala Mountains, Tanzania. J Ethol 1:75–85Google Scholar
  35. Hashimoto C (1997) Context and development of sexual behavior of wild bonobos (Pan paniscus) at Wamba, Zaire. Int J Primatol 18:1–21CrossRefGoogle Scholar
  36. Hashimoto C, Furuichi T (1994) Social role and development of noncopulatory sexual behavior of wild bonobos. In: Wrangham R, McGrew WC, De Waal FBM, Heltne PG (eds) Chimpanzee cultures. Harvard University Press, Cambridge, London, pp 155–168Google Scholar
  37. Hashimoto C, Furuichi T (2006a) Comparison of behavioral sequence of copulation between chimpanzees and bonobos. Primates 47:51–55CrossRefPubMedGoogle Scholar
  38. Hashimoto C, Furuichi T (2006b) Frequent copulations by females and high promiscuity in chimpanzees in the Kalinzu forest, Uganda. In: Newton-Fisher NE, Notman H, Paterson JD, Reynolds V (eds) Primates of western Uganda. Springer, New York, pp 247–257CrossRefGoogle Scholar
  39. 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 107–119CrossRefGoogle Scholar
  40. Hohmann G, Fruth B (2000) Use and function of genital contacts among female bonobos. Anim Behav 59:107–120CrossRefGoogle Scholar
  41. Idani G (1991) Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatol (Basel) 57:83–95CrossRefGoogle Scholar
  42. Kano T (1982) The social group of pygmy chimpanzees (Pan paniscus) of Wamba. Primates 23:171–188CrossRefGoogle Scholar
  43. Kano T (1992) The last ape: pygmy chimpanzee behavior and ecology. Stanford University Press, Palo AltoGoogle Scholar
  44. Kapsalis E, Johnson RL (2006) Getting to know you: female–female consortships in free-ranging rhesus monkeys. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals: an evolutionary perspective. Cambridge University Press, Cambridge, pp 220–237Google Scholar
  45. Koyama N, Takahata Y, Huffman MA, Norikoshi K, Suzuki H (1992) Reproductive parameters of female Japanese macaques: thirty years data from the Arashiyama troops, Japan. Primates 33:33–47Google Scholar
  46. Kuroda S (1980) Social behavior of the pygmy chimpanzees. Primates 21:181–197CrossRefGoogle Scholar
  47. Mann J (2006) Establishing trust: socio-sexual behaviour and the development of male–male bonds among Indian Ocean bottlenose dolphins. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals: an evolutionary perspective. Cambridge University Press, New York, pp 107–130Google Scholar
  48. Matsumoto-Oda A (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behav Ecol Sociobiol 46:258–266CrossRefGoogle Scholar
  49. 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 121–134CrossRefGoogle Scholar
  50. Nadler R (1986) Sex-related behavior of immature wild mountain gorillas. Dev Psychobiol 19(2):125–137CrossRefPubMedGoogle Scholar
  51. Nishida T, Takasaki H, Takahata Y (1990) Demography and reproductive profiles. In: Nishida T (ed) The chimpanzees of the Mahale Mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 63–97Google Scholar
  52. 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 59:99–121CrossRefPubMedGoogle Scholar
  53. Patterson IAP, Reid RJ, Wilson B, Grellier K, Ross HM, Thompson PM (1998) Evidence for infanticide in bottlenose dolphins: an explanation for violent interactions with harbour porpoises? Proc R Soc Lond B 265:1–4CrossRefGoogle Scholar
  54. Plooij FX (1984) The behavioral development of free-living chimpanzee babies and infants. Ablex, NorwoodGoogle Scholar
  55. Pusey A (1990) Behavioral-changes at adolescence in chimpanzees. Behaviour 115:203–246Google Scholar
  56. 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 250–266Google Scholar
  57. Saito C, Sato S, Suzuki S, Sugiura H, Agetsuma N, Takahata Y, Sasaki C, Takahashi H, Tanaka T, Yamagiwa J (1998) Aggressive intergroup encounters in two populations of Japanese macaques (Macaca fuscata). Primates 39:303–312CrossRefGoogle Scholar
  58. Sommer V, Vasey PL (2006) Homosexual behavior in animals. Cambridge University Press, CambridgeGoogle Scholar
  59. Sprague DS (1989) Male intertroop movement during the mating season among the Japanese macaques of Yakushima Island, Japan. A dissertation presented to the Faculty of the Graduate School of Yale UniversityGoogle Scholar
  60. Stevens JMG, Vervaecke H, Van Elsacker L (2008) The bonobo’s adaptive potential: social relations under captive conditions. In: Furuichi T, Thompson J (eds) The bonobos: behavior, ecology, and conservation. Springer, New York, pp 19–38CrossRefGoogle Scholar
  61. Suzuki S, Hill DA, Sprague DS (1998) Intertroop transfer and dominance rank structure of nonnatal male Japanese macaques in Yakushima, Japan. Int J Primatol 19(4):703–722CrossRefGoogle Scholar
  62. Takahata Y (1980) The reproductive biology of a free-ranging troop of Japanese monkeys. Primates 21(3):303–329CrossRefGoogle Scholar
  63. Takahata Y (1982) The socio-sexual behavior of Japanese monkeys. Z Tierpsychol 59:89–108CrossRefPubMedGoogle Scholar
  64. Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Sugiura H, Takahashi H, Yamagiwa J, Izawa K, Furuichi T, Hill DA, Maruhashi T, Saito C, Sato S, Sprague DS (1998) Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: a preliminary report. Primates 39:339–349Google Scholar
  65. Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29–38CrossRefGoogle Scholar
  66. Tutin CEG, McGinnis PR (1981) Chimpanzee reproduction in the wild. In: Graham CE (ed) Reproductive biology of the great apes: comparative and biomedical perspectives. Academic Press, New York, pp 239–264CrossRefGoogle Scholar
  67. Vasey PL (1995) Homosexual behavior in primates: a review of evidence and theory. Int J Primatol 16:173–204CrossRefGoogle Scholar
  68. Vasey PL (2006) The pursuit of pleasure: an evolutionary history of female homosexual behaviour in Japanese macaques. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals. Cambridge University Press, Cambridge, pp 191–219Google Scholar
  69. Wallis J (1997) A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J Reprod Fertil 109:297–307CrossRefPubMedGoogle Scholar
  70. Watanabe K, Mori A (1992) Characteristic features of reproduction of Koshima monkeys, Mucaca fuscata fuscata: a summary of thirty-four years of observation. Primates 33:1–32Google Scholar
  71. Watson-Capps J (2005) Female mating behavior in the context of sexual coercion and female ranging behavior of bottlenose dolphins in Shark Bay, Western Australia. Ph.D. thesis, Georgetown University, Washington, DCGoogle Scholar
  72. Watts DP (2007) Effects of male group size, parity, and cycle stage on female chimpanzee copulation rates at Ngogo, Kibale National Park, Uganda. Primates 48:222–231CrossRefPubMedGoogle Scholar
  73. White FJ (1988) Party composition and dynamics in Pan paniscus. Int J Primatol 9:179–193CrossRefGoogle Scholar
  74. White FJ, Wrangham RW (1988) Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour 105:148–164CrossRefGoogle Scholar
  75. Wrangham RW (1979) Sex differences in chimpanzee dispersion. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 481–489Google Scholar
  76. Wrangham RW (2000) Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 248–258Google Scholar
  77. Wrangham R (2002) The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion? In: Boesch C, Hohmann G, Marchant LF (eds) Behavioral diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 204–215CrossRefGoogle Scholar
  78. Yamagiwa J (2006) Playful encounters: the development of homosexual behaviour in male mountain gorillas. In: Homosexual behaviour in animals: an evolutionary perspective. Cambridge University Press, New York, pp 273–293Google Scholar

Copyright information

© Springer Japan 2014

Authors and Affiliations

  • Takeshi Furuichi
    • 1
  • Richard Connor
    • 2
  • Chie Hashimoto
    • 1
  1. 1.Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Biology DepartmentUMASS-DartmouthNorth DartmouthUSA

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