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Archives of Sexual Behavior

, Volume 47, Issue 4, pp 847–856 | Cite as

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

  • Noëlle Gunst
  • Paul L. Vasey
  • Jean-Baptiste Leca
Original Paper

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.

Keywords

Interspecific sexual behavior Sexual development Learning hypothesis Mate deprivation Reproductive interference 

Notes

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.

References

  1. Abernethy, K. (1994). The establishment of a hybrid zone between red and sika deer (genus Cervus). Molecular Ecology, 3, 551–562.CrossRefPubMedGoogle Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.CrossRefPubMedGoogle Scholar
  3. Bagemihl, B. (1999). Biological exuberance: Animal homosexuality and natural diversity. New York: St. Martin’s Press.Google Scholar
  4. 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
  5. 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.CrossRefGoogle Scholar
  6. Burdfield-Steel, E. R., & Shuker, D. M. (2011). Reproductive interference. Current Biology, 21, R450–R451.CrossRefPubMedGoogle Scholar
  7. Cohen, J. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement, 20, 37–46.CrossRefGoogle Scholar
  8. Cothran, R. D. (2015). The importance of reproductive interference in ecology and evolution: From organisms to communities. Population Ecology, 57, 339–341.CrossRefGoogle Scholar
  9. Dame, E. A., & Petren, K. (2006). Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Animal Behaviour, 71, 1165–1173.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans. Oxford: Oxford University Press.CrossRefGoogle Scholar
  13. Enomoto, T. (1974). The sexual behavior of Japanese monkeys. Journal of Human Evolution, 3, 351–372.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. Gröning, J., & Hochkirch, A. (2008). Reproductive interference between animal species. Quarterly Review of Biology, 83, 257–282.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. Hayward, J. L. (2003). Sexual aggression by a male north-ern elephant seal on harbor seal pups in Washington. Northwestern Naturalist, 84, 148–150.CrossRefGoogle Scholar
  22. Koda, H. (2012). Possible use of heterospecific food-associated calls of macaques by sika deer for foraging efficiency. Behavioural Processes, 91, 30–34.CrossRefPubMedGoogle Scholar
  23. Kyogoku, D. (2015). Reproductive interference: Ecological and evolutionary consequences of interspecific promiscuity. Population Ecology, 57, 253–260.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Leca, J.-B., Gunst, N., & Vasey, P. L. (2014b). Development of sexual behavior in free-ranging female Japanese macaques. Developmental Psychobiology, 56, 1199–1213.PubMedGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. McCullough, D. R., Takatsuki, S., & Kaji, K. (2009). Sika deer: Biology and management of native and introduced populations. Tokyo: Springer.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. Pfennig, K. S. (2007). Facultative mate choice drives adaptive hybridization. Science, 318, 965–967.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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
  38. 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.CrossRefGoogle Scholar
  39. Vasey, P. L., & Duckworth, N. (2008). Female-male mounting in Japanese macaques: The proximate role of sexual reward. Behavioural Processes, 77, 405–407.CrossRefPubMedGoogle Scholar
  40. 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.PubMedGoogle Scholar
  41. 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
  42. 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.CrossRefPubMedGoogle Scholar
  43. Yamaguchi, R., & Iwasa, Y. (2015). Reproductive interference can promote recurrent speciation. Population Ecology, 57, 343–346.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Noëlle Gunst
    • 1
  • Paul L. Vasey
    • 1
  • Jean-Baptiste Leca
    • 1
  1. 1.Department of PsychologyUniversity of LethbridgeLethbridgeCanada

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