Abstract
Among non-human primates, male dominance rank is not necessarily a good indicator of mating success, and relationships between male dominance rank and mating or reproductive success are affected by female behavior and sexual states implying their probability of conception. Although comparisons of the behavior of male chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) suggest that the effect of male dominance rank on mating success is expected to be less prominent in bonobos, recent genetic studies have shown that high-ranking male reproductive skew is higher in bonobos than in chimpanzees. One possible reason for the higher reproductive skew in bonobos could be that female behavior and their sexual states may have much more influence on male mating and reproductive success in bonobos than in chimpanzees. In the current study on bonobos, we conducted focal animal observation of females and analyzed the influence of female sexual swelling, the number of days after parturition, and dominance rank of males on female associations, and copulation with adult males. Our results showed that females with maximum swelling (MS) had more proximity with high-ranking males and copulated more frequently with higher-ranking males than with lower-ranking males. Females for whom longer time had elapsed since parturition, and therefore had higher probabilities of conception, had 5-m proximity with adult males more frequently than females whom shorter time had elapsed since parturition, but did not have more copulation with adult males. Females with MS had proximity and copulated with high-ranking males frequently, which partly explains why the reproductive skew is so high in bonobos. These results are discussed in relation to previous hypotheses on the influence of long-lasting mother–son relationships on mating success of males and on the contribution of female receptivity during non-conceptive nursing periods to moderate intermale aggression in bonobos.
Similar content being viewed by others
Change history
01 September 2022
A Correction to this paper has been published: https://doi.org/10.1007/s10329-022-01014-z
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196. https://doi.org/10.1016/j.anbehav.2006.05.001
Alberts SC (2012) Magnitude and sources of variation in male reproductive performance. In: Mitani J, Call J, Kappeler P et al (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 412–431
Alfaro JWL (2005) Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus). Am J Primatol 67:313–328. https://doi.org/10.1002/ajp.20188
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Berard J (1999) A Four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta). Primates 40:159–175
Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130:103–115. https://doi.org/10.1002/ajpa.20341
Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885. https://doi.org/10.1126/science.1133311
Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056. https://doi.org/10.1016/S0003-3472(05)80642-6
Curie-Cohen M, Yoshihara D, Luttrell L et al (1983) The effects of dominance on mating behavior and paternity in a captive troop of rhesus monkeys (Macaca mulatta). Am J Primatol 5:127–138. https://doi.org/10.1002/ajp.1350050204
De RJ, Van HJ (1993) Male dominance rank and reproductive success in primate groups. Primates 34:513–523
Dixson AF (1998) Primate sexuality: Comparative studies of the prosimians, monkeys, apes and human beings. Oxford University Press, Oxford
Douglas B, Martin M, Ben B (2012) lme4: linear mixed-effects models using S4 classes. R Studio, Boston, MA
Douglas PH, Hohmann G, Murtagh R et al (2016) Mixed messages: wild female bonobos show high variability in the timing of ovulation in relation to sexual swelling patterns. BMC Evol Biol 16:2–4. https://doi.org/10.1186/s12862-016-0691-3
Douglas PH, Ngonga Ngomo AC, Hohmann G (2017) A novel approach for dominance assessment in gregarious species: ADAGIO. Anim Behav 123:21–32. https://doi.org/10.1016/j.anbehav.2016.10.014
Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333. https://doi.org/10.1016/0162-3095(95)00050-U
Fox J, Weisberg S (2018) An R companion to applied regression, 3rd edn. SAGE, Thousand Oaks
Furuichi T (1987) Sexual swelling, receptivity, and grouping of wild pygmy chimpanzees females at Wamba, Zaire. Primates 28:309–318
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 (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 18:855–875. https://doi.org/10.1023/A:1026327627943
Furuichi T (2011) Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20:131–142. https://doi.org/10.1002/evan.20308
Furuichi T, Hashimoto C (2002) Why female bonobos have a lower copulation rate during estrus than chimpanzees. In: Boesch C, Hohmann G, Marchant L (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 156–167
Furuichi T, Ihobe H (1994) Variation in male relationships in bonobos and chimpanzees. Behaviour 130:211–228
Furuichi T, Idani G, Ihobe H et al (2012) Long-term studies on wild bonobos at Wamba, Luo scientific reserve, DR Congo: towards the understanding of female life history in a male-philopatric species. In: Kappeler P, Watts D (eds) Long-term field studies of primates. Springer, Berlin Heidelberg, pp 413–433
Furuichi T, Connor R, Hashimoto C (2014) Non-conceptive sexual interactions in monkeys, apes, and dolphins. In: Yamagiwa J, Karczmarski L (eds) Primates and cetaceans: field research and conservation of complex mammalian societies. Springer, Tokyo, pp 385–408
Goodall J (1968) The behaviour of free-living chimpanzees in the Gombe stream reserve. Anim Behav Monogr 1:161–311. https://doi.org/10.1016/s0066-1856(68)80003-2
Hashimoto C (1997) Context and development of sexual behavior of wild bonobos (Pan paniscus) at Wamba, Zaire. Int J Primatol 18:1–21. https://doi.org/10.1023/A:1026384922066
Hashimoto C, Ryu H, Mouri K et al (2022) Physical, behavioral, and hormonal changes in the resumption of sexual receptivity during postpartum infertility in female bonobos at Wamba. Primates 63:109–121. https://doi.org/10.1007/S10329-021-00968-W/FIGURES/4
Hashimoto C, Tashiro Y, Hibino E, et al (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. Developments in Primatology: Progress and Prospects. Springer New York, pp 107–119
Hohmann G, Fruth B (2003) Intra- and inter-sexual aggression by bonobos in the context of mating. Behaviour 1389–1413
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
Inoue M, Takenaka A, Tanaka S et al (1990) Paternity discrimination in a Japanese macaque group by DNA fingerprinting. Primates 31:563–570. https://doi.org/10.1007/BF02382539
Ishizuka S, Kawamoto Y, Sakamaki T et al (2018) Paternity and kin structure among neighbouring groups in wild bonobos at Wamba. R Soc Open Sci 5(171006):171006. https://doi.org/10.1098/rsos.171006
Kano T (1992) The last ape: pygmy chimpanzee behavior and ecology. Stanford University Press, Stanford
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740
Keddy-Hector AC (1992) Mate choice in non-human primates. Am Zool 32:62–70. https://doi.org/10.1093/icb/32.1.62
Kuroda S (1980) Social behavior of the pygmy chimpanzees. Primates 21:181–197
Kutsukake N, Nunn CL (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behav Ecol Sociobiol 60:695–706. https://doi.org/10.1007/s00265-006-0213-1
Leroux M, Bosshard AB, Chandia B et al (2021) Chimpanzees combine pant hoots with food calls into larger structures. Anim Behav 179:41–50. https://doi.org/10.1016/J.ANBEHAV.2021.06.026
Majolo B, Lehmann J, de Bortoli VA, Schino G (2012) Fitness-related benefits of dominance in primates. Am J Phys Anthropol 147:652–660. https://doi.org/10.1002/ajpa.22031
Matsumoto-Oda A (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthil) at Mahale. Behav Ecol Sociobiol 46:258–266. https://doi.org/10.1007/s002650050618
Mulavwa M, Furuichi T, Yangozene K et al (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
Mulavwa MN, Yangozene K, Yamba-Yamba M et al (2010) Nest groups of wild bonobos at Wamba: Selection of vegetation and tree species and relationships between nest group size and party size. Am J Primatol 72:575–586. https://doi.org/10.1002/ajp.20810
Muller MN, Mitani JC (2005) Conflict and cooperation in wild chimpanzees. Adv Study Behav 35:275–331. https://doi.org/10.1016/S0065-3454(05)35007-8
Mundry R, Numm CL (2009) Stepwise model fitting and statistical inference: turning noise into signal pollution. Am Nat 173:119–123
Newton-Fisher NE (2004) Hierarchy and social status in Budongo chimpanzees. Primates 45:81–87. https://doi.org/10.1007/s10329-003-0064-6
Newton-Fisher NE, Thompson ME, Reynolds V et al (2010) Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda. Am J Phys Anthropol 142:417–428. https://doi.org/10.1002/ajpa.21241
Nishida T (1979) The social structure of chimpanzees of the Mahale Mountains. In: Hamburg D, McCown E (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 72–121
Parish AR (1996) Female relationships in bonobos (Pan paniscus): evidence for bonding, cooperation, and female dominance in a male-philopatric species. Hum Nat 7:61–96. https://doi.org/10.1007/BF02733490
Parish AR, de Waal FBM (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 907:97–113. https://doi.org/10.1111/j.1749-6632.2000.tb06618.x
Paul A, Kuester J, Timme A, Arnemann J (1993) The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates 34:491–502. https://doi.org/10.1007/BF02382660
Peter MK (2012) Mate choice. In: Mitani J, Call J, Kappeler P et al (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 367–386
Pieta K (2008) Female mate preferences among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda. Int J Primatol 29:845–864. https://doi.org/10.1007/s10764-008-9282-5
Reichert KE, Heistermann M, Hodges JK et al (2002) What females tell males about their reproductive status: are morphological and behavioural cues reliable signals of ovulation in bonobos (Pan paniscus)? Ethology 108:583–600. https://doi.org/10.1046/j.1439-0310.2002.00798.x
Ryu H, Hill DA, Furuichi T (2015) Prolonged maximal sexual swelling in wild bonobos facilitates affiliative interactions between females. Behaviour 152:285–311. https://doi.org/10.1163/1568539X-00003212
Ryu H, Hashimoto C, David A et al (2022) Do males know? Evidence-driven rainmaking mating strategy by male bonobos to meet the fertile window of females. bioRxiv. https://doi.org/10.1101/2022.03.13.483391
Sakamaki T, Behncke I, Laporte M 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: life history and social strategies in male-philopatric species. Springer, Tokyo, pp 127–164
Sakamaki T, Ryu H, Toda K et al (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
Small MF (1989) Female choice in nonhuman primates. Am J Phys Anthropol 32:103–127. https://doi.org/10.1002/ajpa.1330320506
Stumpf RM, Boesch C (2005) Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d’Ivoire. Behav Ecol Sociobiol 57:511–524. https://doi.org/10.1007/s00265-004-0868-4
Stumpf RM, Boesch C (2006) The efficacy of female choice in chimpanzees of the Taï forest, Côte d’Ivoire. Behav Ecol Sociobiol 60:749–765. https://doi.org/10.1007/s00265-006-0219-8
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
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 Biol Sci 278:590–598. https://doi.org/10.1098/rspb.2010.1572
Surbeck M, Boesch C, Girard-Buttoz C et al (2017a) Comparison of male conflict behavior in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), with specific regard to coalition and post-conflict behavior. Am J Primatol 79:1–11. https://doi.org/10.1002/ajp.22641
Surbeck M, Langergraber KE, Fruth B et al (2017b) Male reproductive skew is higher in bonobos than chimpanzees. Curr Biol 27:R640–R641. https://doi.org/10.1016/j.cub.2017.05.039
Surbeck M, Girard-Buttoz C, Samuni L et al (2021) Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees. Commun Biol 4:1119. https://doi.org/10.1038/s42003-021-02641-w
Takahata Y, Huffman MA, Suzuki S et al (1999) Why dominants do not consistently attain high mating and reproductive success: a review of longitudinal Japanese macaque studies. Primates 40:143–158. https://doi.org/10.1007/BF02557707
Terada S, Nackoney J, Sakamaki T et al (2015) Habitat use of bonobos (Pan paniscus) at Wamba: selection of vegetation types for ranging, feeding, and night-sleeping. Am J Primatol 77:701–713. https://doi.org/10.1002/ajp.22392
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/s10764-020-00151-w
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
Toyoda A, Maruhashi T, Malaivijitnond S et al (2022) Mating and reproductive success in free-ranging stump-tailed macaques: effectiveness of male-male coalition formation as a reproductive strategy. Front Ecol Evol 10:802012. https://doi.org/10.3389/fevo.2022.802012
Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29–38. https://doi.org/10.1007/BF00293242
Watts DP (1998) Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav Ecol Sociobiol 44:43–55. https://doi.org/10.1007/s002650050513
White FJ (1992) Pygmy chimpanzee social organization: Variation with party size and between study sites. Am J Primatol 26:203–214. https://doi.org/10.1002/ajp.1350260306
Wrangham RW (1993) The evolution of sexuality in chimpanzees and bonobos. Hum Nat 4:47–79. https://doi.org/10.1007/BF02734089
Wroblewski EE, Murray CM, Keele BF et al (2009) Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 77:873–885. https://doi.org/10.1016/j.anbehav.2008.12.014
Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer Science+Business Media, New York
Acknowledgments
We thank the Research Center for Ecology and Forestry and the Ministry of Scientific Research, DRC. We also thank members of the Ecology and Social Behavior section of the Primate Research Institute, Kyoto University, for their helpful advice, and our research assistants at Wamba for their great help during the bonobo observations. We thank Ms. Keiko Mouri and Dr. Chie Hashimoto for helping with our hormonal analysis. We are grateful to Mr. Shohei Shibata, Dr. Shintaro Ishizuka, Dr. Kazuya Toda, Dr. Heungjin Ryu, Dr. Nahoko Tokuyama, and Dr. Tetsuya Sakamaki, for providing valuable information, contributing to the continuous observation of the study group and camp management at Wamba.
Funding
This study was supported by the Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (26257408, 16H02753, and 18KK0204 to Yokoyama).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Yokoyama, T., Furuichi, T. Why bonobos show a high reproductive skew towards high-ranking males: analyses for association and mating patterns concerning female sexual states. Primates 63, 483–494 (2022). https://doi.org/10.1007/s10329-022-01004-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-022-01004-1