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Deer Mates: A Quantitative Study of Heterospecific Sexual Behaviors Performed by Japanese Macaques Toward Sika Deer

Archives of Sexual Behavior volume 47, pages 847–856 (2018)Cite this article

Abstract

This is the first quantitative study of heterospecific sexual behavior between a non-human primate and a non-primate species. We observed multiple occurrences of free-ranging adolescent female Japanese macaques (Macaca fuscata) performing mounts and sexual solicitations toward sika deer (Cervus nippon) at Minoo, central Japan. Our comparative description of monkey-deer versus monkey-monkey interactions supported the “heterospecific sexual behavior” hypothesis: the mounts and demonstrative solicitations performed by adolescent female Japanese macaques toward sika deer were sexual in nature. In line with our previous research on the development of homospecific sexual behavior in immature female Japanese macaques, this study will allow us to test other hypotheses in the future, such as the “practice for homospecific sex,” the “safe sex,” the “homospecific sex deprivation,” the “developmental by-product,” and the “cultural heterospecific sex” hypotheses. Further research will be necessary to ascertain whether this group-specific sexual behavior was a short-lived fad or an incipient cultural phenomenon and may also contribute to better understanding the proximate and ultimate causes of reproductive interference.

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Notes

  1. Bagemihl (1999) provided an anecdotal account of a captive female rhesus macaque who sexually solicited a dog.

References

  • Abernethy, K. (1994). The establishment of a hybrid zone between red and sika deer (genus Cervus). Molecular Ecology, 3, 551–562.

    Article  PubMed  Google Scholar 

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.

    Article  PubMed  Google Scholar 

  • Bagemihl, B. (1999). Biological exuberance: Animal homosexuality and natural diversity. New York: St. Martin’s Press.

    Google Scholar 

  • Bergman, T. J., & Beehner, J. C. (2003). Hybrid zones and sexual selection: Insights from the Awash baboon hybrid zone (Papio hamadryas anubis x P. h. hamadryas). In C. Jones (Ed.), Sexual selection and primates: New insights and directions (pp. 500–537). Norman, OK: American Society of Primatologists.

    Google Scholar 

  • Best, P. B., Meyer, M. A., & Weeks, R. W. (1981). Interactions between a male elephant seal (Mirounga leonina) and cape fur seals (Arctocephalus pusillus). South African Journal of Zoology, 16, 59–66.

    Article  Google Scholar 

  • Burdfield-Steel, E. R., & Shuker, D. M. (2011). Reproductive interference. Current Biology, 21, R450–R451.

    Article  PubMed  Google Scholar 

  • Cohen, J. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement, 20, 37–46.

    Article  Google Scholar 

  • Cothran, R. D. (2015). The importance of reproductive interference in ecology and evolution: From organisms to communities. Population Ecology, 57, 339–341.

    Article  Google Scholar 

  • Dame, E. A., & Petren, K. (2006). Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Animal Behaviour, 71, 1165–1173.

    Article  Google Scholar 

  • De Bruyn, P. J. N., Tosh, C. A., & Bester, M. N. (2008). Sexual harassment of a king penguin by an Antarctic fur seal. Journal of Ethology, 26, 295–297.

    Article  Google Scholar 

  • Deering, M. D., & Scriber, J. M. (2002). Field bioassays show heterospecific mating preference asymmetry between hybridizing North American Papilio butterfly species (Lepidoptera: Papilionidae). Journal of Ethology, 20, 25–33.

    Article  Google Scholar 

  • Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Enomoto, T. (1974). The sexual behavior of Japanese monkeys. Journal of Human Evolution, 3, 351–372.

    Article  Google Scholar 

  • Fitzpatrick, B. M., & Shaffer, H. B. (2007). Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proceedings of the National Academy of Sciences USA, 104, 15793–15798.

    Article  Google Scholar 

  • Fujimoto, H., Hiramatsu, T., & Takafuji, A. (1996). Reproductive interference between Panonychus mori and P. citri (Acari: Tetranychidae) in peach orchards. Applied Entomology and Zoology, 31, 59–65.

    Article  Google Scholar 

  • Gröning, J., & Hochkirch, A. (2008). Reproductive interference between animal species. Quarterly Review of Biology, 83, 257–282.

    Article  PubMed  Google Scholar 

  • Gunst, N., Leca, J.-B., & Vasey, P. L. (2013). Development of sexual and socio-sexual behaviours in free-ranging juvenile male Japanese macaques, Macaca fuscata. Behaviour, 150, 1225–1254.

    Article  Google Scholar 

  • Gunst, N., Leca, J.-B., & Vasey, P. L. (2015). Influence of sexual competition and social context on homosexual behavior in adolescent female Japanese macaques. American Journal of Primatology, 77, 502–515.

    Article  PubMed  Google Scholar 

  • Haddad, W. A., Reisinger, R. R., Scott, T., Bester, M. N., & de Bruyn, P. J. N. (2015). Multiple occurrences of king penguin (Aptenodytes patagonicus) sexual harassment by Antarctic fur seals (Arctocephalus gazella). Polar Biology, 38, 741–746.

    Article  Google Scholar 

  • Hatfield, B. B., Jameson, R. J., Murphey, T. G., & Woodard, D. D. (1994). Atypical interactions between male southern sea otters and pinnipeds. Marine Mammal Science, 10, 111–114.

    Article  Google Scholar 

  • Hayward, J. L. (2003). Sexual aggression by a male north-ern elephant seal on harbor seal pups in Washington. Northwestern Naturalist, 84, 148–150.

    Article  Google Scholar 

  • Koda, H. (2012). Possible use of heterospecific food-associated calls of macaques by sika deer for foraging efficiency. Behavioural Processes, 91, 30–34.

    Article  PubMed  Google Scholar 

  • Kyogoku, D. (2015). Reproductive interference: Ecological and evolutionary consequences of interspecific promiscuity. Population Ecology, 57, 253–260.

    Article  Google Scholar 

  • Leca, J.-B., Gunst, N., Ottenheimer Carrier, L., & Vasey, P. L. (2014a). Inter-group variation in non-conceptive sexual activity in female Japanese macaques: Could it be cultural? Animal Behavior & Cognition, 1, 387–409.

    Article  Google Scholar 

  • Leca, J.-B., Gunst, N., & Vasey, P. L. (2014b). Development of sexual behavior in free-ranging female Japanese macaques. Developmental Psychobiology, 56, 1199–1213.

    PubMed  Google Scholar 

  • Leca, J.-B., Gunst, N., & Vasey, P. L. (2014c). Male homosexual behavior in a free-ranging all-male group of Japanese macaques at Minoo, Japan. Archives of Sexual Behavior, 43, 853–861.

    Article  PubMed  Google Scholar 

  • Leca, J.-B., Gunst, N., & Vasey, P. L. (2015). Comparative development of heterosexual and homosexual behaviors in free-ranging female Japanese macaques. Archives of Sexual Behavior, 44, 1215–1231.

    Article  PubMed  Google Scholar 

  • Majolo, B., & Ventura, R. (2004). Apparent feeding association between Japanese macaques (Macaca fuscata yakui) and sika deer (Cervus nippon) living on Yakushima island, Japan. Ethology Ecology & Evolution, 16, 33–40.

    Article  Google Scholar 

  • McCullough, D. R., Takatsuki, S., & Kaji, K. (2009). Sika deer: Biology and management of native and introduced populations. Tokyo: Springer.

    Book  Google Scholar 

  • McGowan, C., & Davidson, W. S. (1992). Unidirectional hybridization between brown trout (Salmo trutta) and Atlantic salmon (S. salar) in Newfoundland. Canadian Journal of Fisheries and Aquatic Sciences, 49, 1953–1958.

    Article  Google Scholar 

  • Miller, E. H., Ponce de Leon, A., & DeLong, R. L. (1996). Violent interspecific sexual behavior by male sea lions (Otariidae): Evolutionary and phylogenetic implications. Marine Mammal Science, 12, 468–476.

    Article  Google Scholar 

  • Nishikawa, M., & Mochida, K. (2010). Coprophagy-related interspecific nocturnal interactions between Japanese macaques (Macaca fuscata yakui) and sika deer (Cervus Nippon yakushimae). Primates, 51, 95–99.

    Article  PubMed  Google Scholar 

  • Pelé, M., Bonnefoy, A., Shimada, M., & Sueur, C. (2017). Interspecies sexual behaviour between a male Japanese macaque and female sika deer. Primates, 58, 275–278.

    Article  Google Scholar 

  • Pfennig, K. S. (2007). Facultative mate choice drives adaptive hybridization. Science, 318, 965–967.

    Article  PubMed  Google Scholar 

  • Rhymer, J. M., Williams, M. J., & Braun, M. J. (1994). Mitochondrial analysis of gene flow between New Zealand mallards (Anas platyrhynchos) and grey ducks (A. superciliosa). Auk, 111, 970–978.

    Article  Google Scholar 

  • Schultz, J. K., & Switzer, P. V. (2001). Pursuit of heterospecific targets by territorial amberwing dragonflies (Perithemis tenera Say): A case of mistaken identity. Journal of Insect Behavior, 14, 607–620.

    Article  Google Scholar 

  • Shimizu, K. (2012). Birth control in female Japanese macaques at Iwatayama Monkey Park, Arashiyama. In J.-B. Leca, M. A. Huffman, & P. L. Vasey (Eds.), The monkeys of stormy mountain: 60 years of primatological research on the Japanese macaques of Arashiyama (pp. 435–452). Cambridge: Cambridge University Press.

    Google Scholar 

  • Tsuji, Y., Shimoda-Ishiguro, M., Ohnishi, N., & Takatsuki, S. (2007). A friend in need is a friend indeed: Feeding association between Japanese macaques and sika deer. Acta Theriologica, 52, 427–434.

    Article  Google Scholar 

  • Vasey, P. L., & Duckworth, N. (2008). Female-male mounting in Japanese macaques: The proximate role of sexual reward. Behavioural Processes, 77, 405–407.

    Article  PubMed  Google Scholar 

  • Vasey, P. L., Foroud, A., Duckworth, N., & Kovacovsky, S. D. (2006). Male-female and female-female mounting in Japanese macaques: A comparative analysis of posture and movement. Archives of Sexual Behavior, 35, 117–129.

    PubMed  Google Scholar 

  • Vasey, P. L., & VanderLaan, D. P. (2012). Is female homosexual behaviour in Japanese macaques truly sexual? In J.-B. Leca, M. A. Huffman, & P. L. Vasey (Eds.), The monkeys of stormy mountain: 60 years of primatological research on the Japanese macaques of Arashiyama (pp. 153–172). Cambridge: Cambridge University Press.

    Google Scholar 

  • Wallen, K. (1996). Nature needs nurture: The interaction of hormonal and social influences on the development of behavioral sex differences in rhesus monkeys. Hormones and Behavior, 30, 364–378.

    Article  PubMed  Google Scholar 

  • Yamaguchi, R., & Iwasa, Y. (2015). Reproductive interference can promote recurrent speciation. Population Ecology, 57, 343–346.

    Article  Google Scholar 

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Acknowledgements

This study was funded by the following agencies: Natural Sciences and Engineering Research Council of Canada (NSERC), Alberta Innovates Health Solutions (AIHS), Japan Society for the Promotion of Science (JSPS), American Institute of Bisexuality (AIB), the L.S.B. Leakey Foundation, as well as the Office of the Dean of Arts and Science and the Office of Research Services at the University of Lethbridge. We thank John R. Sylla from the AIB and Penny D’Agnone for help securing AIHS funding. We thank Y. Iwanaga for permission to work at Meiji Memorial Forest Minoo Park and S. Suzuki for valuable information in the field. We thank the Enomoto family of Arashiyama for logistical support in Japan. We thank the Editor and two anonymous reviewers for fruitful comments on a previous version of the article.

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Authors and Affiliations

  1. Department of Psychology, University of Lethbridge, 4401 University Drive, Lethbridge, AB, T1K 3M4, Canada

    Noëlle Gunst, Paul L. Vasey & Jean-Baptiste Leca

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  1. Noëlle Gunst
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  2. Paul L. Vasey
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  3. Jean-Baptiste Leca
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Correspondence to Noëlle Gunst.

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Gunst, N., Vasey, P.L. & Leca, JB. Deer Mates: A Quantitative Study of Heterospecific Sexual Behaviors Performed by Japanese Macaques Toward Sika Deer. Arch Sex Behav 47, 847–856 (2018). https://doi.org/10.1007/s10508-017-1129-8

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  • DOI: https://doi.org/10.1007/s10508-017-1129-8

Keywords

  • Interspecific sexual behavior
  • Sexual development
  • Learning hypothesis
  • Mate deprivation
  • Reproductive interference