Abstract
Urine is involved in sexual communication in New World monkeys and lemurs, but most studies of the role of olfaction in sexual communication in Old World monkeys have focused on vaginal secretions rather than urine. We investigated whether female urine promotes male sexual behaviors (approaches and inspections of genital area) in Japanese macaques (Macaca fuscata). We used a sequential presentation paradigm in behavioral experiments, presenting unfamiliar female urine and control cotton swabs to males living in a social group with cycling females. We tested whether males (N = 3) showed more processing behaviors (licking, sniffing, tasting) toward female urine (22 stimuli per male from prefertile, fertile, and postfertile phases, based on urinary estrone and progesterone conjugate profiles) than control odor (8 stimuli per male). We then compared male sexual behaviors toward resident females pre- and post-exposure to stimuli and in relation to the females’ reproductive status (perifertile, nonfertile, and pregnancy periods, based on fecal estrone and progesterone conjugate profiles). We found that males showed significantly more processing behaviors toward urine stimuli than to controls but that male behavior did not vary across urine samples from prefertile, fertile, and postfertile phases. Exposure to unfamiliar female urine stimuli did not modulate male approaches to and inspections of resident females at any stage of the female reproductive cycle. Although our study is limited by its small sample size, the results suggest that female urine contains compounds that males detect, but we found no evidence that female urine is related to male sexual behaviors.
Similar content being viewed by others
References
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3), 227–267.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1). doi:10.18637/jss.v067.i01.
Behboodi, E., Katz, D., Samuels, S., Tell, L., Hendrickx, A., & Lasley, B. (1991). The use of a urinary estrone conjugates assay for detection of optimal mating time in the cynomolgus macaque (Macaca fascicularis). Journal of Medical Primatology, 20(5), 229–234.
Brauch, K., Pfefferle, D., Hodges, K., Möhle, U., Fischer, J., & Heistermann, M. (2007). Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Hormones and Behavior, 52(3), 375–383.
Cerda-Molina, A. L., Hernández-López, L., Chavira, R., Cárdenas, M., Paez-Ponce, D., et al (2006a). Endocrine changes in male stumptailed macaques (Macaca arctoides) as a response to odor stimulation with vaginal secretions. Hormones and Behavior, 49(1), 81–87.
Cerda-Molina, A. L., Hernández-López, L., Rojas-Maya, S., Murcia-Mejía, C., & Mondragón-Ceballos, R. (2006b). Male-induced sociosexual behavior by vaginal secretions in Macaca arctoides. International Journal of Primatology, 27(3), 791–807.
Cerda-Molina, A. L., Hernández-López, L., de la O, C. E., Chavira-Ramírez, R., & Mondragón-Ceballos, R. (2013). Changes in men’s salivary testosterone and cortisol levels, and in sexual desire after smelling female axillary and vulvar scents. Frontiers in Endocrinology, 4, 159.
Charpentier, M. J. E., Mboumba, S., Ditsoga, C., & Drea, C. M. (2013). Nasopalatine ducts and flehmen behavior in the mandrill: Reevaluating olfactory communication in Old World primates. American Journal of Primatology, 75(7), 703–714.
Clarke, P. M. R., Barrett, L., & Henzi, S. P. (2009). What role do olfactory cues play in chacma baboon mating? American Journal of Primatology, 71(6), 493–502.
Converse, L. J., Carlson, A. A., Ziegler, T. E., & Snowdon, C. T. (1995). Communication of ovulatory state to mates by female pygmy marmosets, Cebuella pygmaea. Animal Behaviour, 49(3), 615–621.
Crawford, J. C., & Drea, C. M. (2015). Baby on board: Olfactory cues indicate pregnancy and fetal sex in a non-human primate. Biology Letters, 11(2), 20140831.
Curtis, R. F., Ballantine, J. A., Keverne, E. B., Bonsall, R. W., & Michael, R. P. (1971). Identification of primate sexual pheromones and the properties of synthetic attractants. Nature, 232(5310), 396–398.
Dixson, A. F. (1998). Primate sexuality: Comparative studies of the prosimians, monkeys, apes and human beings. New York: Oxford University Press.
Dixson, A. F., & Anderson, M. J. (2002). Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatologica, 73(2–3), 63–69.
Drea, C. M. (2015). D’scent of man: A comparative survey of primate chemosignaling in relation to sex. Hormones and Behavior, 68, 117–133.
Drea, C. M., Boulet, M., Delbarco-Trillo, J., Greene, L. K., Sacha, C. R., et al (2013). The “secret” in secretions: Methodological considerations in deciphering primate olfactory communication. American Journal of Primatology, 75(7), 621–642.
Dubuc, C., Brent, L. J. N., Accamando, A. K., Gerald, M. S., MacLarnon, A., et al (2009). Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. International Journal of Primatology, 30(6), 777–789.
Eaton, G. G., Slob, A., & Resko, J. A. (1973). Cycles of mating behaviour, oestrogen and progesterone in the thick-tailed bushbaby (Galago crassicaudatus crassicaudatus) under laboratory conditions. Animal Behaviour, 21(2), 309–315.
Engelhardt, A., Hodges, J. K., Niemitz, C., & Heistermann, M. (2005). Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Hormones and Behavior, 47(2), 195–204.
Enomoto, T. (1974). The sexual behavior of Japanese monkeys. Journal of Human Evolution, 3(5), 351–372.
Evans, C. S., & Goy, R. W. (1968). Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). Journal of Zoology, 156(2), 181–197.
Ferris, C. F., Snowdon, C. T., King, J. A., Duong, T. Q., Ziegler, T. E., et al (2001). Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues. NeuroReport, 12(10), 2231–2236.
Foerg, R. (1982). Reproductive behavior in Varecia variegata. Folia Primatologica, 38(1–2), 108–121.
Fooden, J., & Aimi, M. (2003). Birth-season variation in Japanese macaques, Macaca fuscata. Primates, 44(2), 109–117.
Fournier, D. A., Skaug, H. J., Ancheta, J., Ianelli, J., Magnusson, A., et al (2012). AD Model Builder: Using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods and Software, 27(2), 233–249.
Fox, G. J. (1982). Potentials for pheromones in chimpanzee vaginal fatty acids. Folia Primatologica, 37(3–4), 255–266.
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. American Journal of Primatology, 53(4), 167–176.
Garcia, C., Shimizu, K., & Huffman, M. (2009). Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). American Journal of Primatology, 71(10), 868–879.
Garcia, C., Huffman, M. A., Shimizu, K., & Speakman, J. R. (2011). Energetic consequences of seasonal breeding in female Japanese macaques (Macaca fuscata). American Journal of Physical Anthropology, 146(2), 161–170.
Go, M. (2009). Seasonal changes in food resource distribution and feeding sites selected by Japanese macaques on Koshima Islet, Japan. Primates, 51(2), 149–158.
Goldfoot, D. A., Kravetz, M. A., Goy, R. W., & Freeman, S. K. (1976). Lack of effect of vaginal lavages and aliphatic acids on ejaculatory responses in rhesus monkeys: Behavioral and chemical analyses. Hormones and Behavior, 7(1), 1–27.
Heistermann, M., Brauch, K., Möhle, U., Pfefferle, D., Dittami, J., & Hodges, K. (2007). Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. American Journal of Primatology, 70(1), 44–53.
Hennessy, M. B., Coe, C. L., Mendoza, S. P., Lowe, E. L., & Levine, S. (1978). Scent-marking and olfactory investigatory behavior in the squirrel monkey (Saimiri sciureus). Behavioral Biology, 24(1), 57–67.
Higham, J. P., Heistermann, M., Ross, C., Semple, S., & Maclarnon, A. (2008). The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates, 49(4), 295–299.
Hill, D. A. (1997). Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima. American Journal of Primatology, 43(4), 305–320.
Hodges, J. K., & Heistermann, M. (2011). Field endocrinology: Monitoring hormonal changes in free-ranging primates. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology: A practical guide. Cambridge: Cambridge University Press.
Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H., et al. (2001). Individual recognition in mice mediated by major urinary proteins. Nature, 414(6864), 631–634.
Iwamoto, T. (1982). Food and nutritional condition of free ranging Japanese monkeys on Koshima Islet during winter. Primates, 23(2), 153–170.
Johnston, R.E., Derzie, A., Chiang, G., Jernigan, P., Lee, H.-C. (1993) Individual scent signatures in golden hamsters: evidence for specialization of function. Animal Behaviour, 45(6), 1061–1070.
Keverne, E. B., & Michael, R. P. (1971). Sex-attractant properties of ether extracts of vaginal secretions from rhesus monkeys. Journal of Endocrinology, 51(2), 313–322.
Klein, L. L. (1971). Observations on copulation and seasonal reproduction of two species of spider monkeys, Ateles belzebuth and A. geoffroyi. Folia Primatologica, 15(3–4), 233–248.
Maestripieri, D., Leoni, M., Raza, S. S., Hirsch, E. J., & Whitham, J. C. (2005). Female copulation calls in Guinea baboons: Evidence for postcopulatory female choice? International Journal of Primatology, 26(4), 737–758.
Matsumoto-Oda, A., Oda, R., Hayashi, Y., Murakami, H., Maeda, N., et al (2003). Vaginal fatty acids produced by chimpanzees during menstrual cycles. Folia Primatologica, 74(2), 75–79.
Michael, R. P., & Keverne, E. B. (1970). Primate sex pheromones of vaginal origin. Nature, 225(5227), 84–85.
Michael, R. P., & Zumpe, D. (1982). Influence of olfactory signals on the reproductive behaviour of social groups of rhesus monkeys (Macaca mulatta). Journal of Endocrinology, 95(2), 189–205.
Michael, R. P., Keverne, E. B., & Bonsall, R. W. (1971). Pheromones: Isolation of male sex attractants from a female primate. Science, 172(3986), 964–966.
Michael, R. P., Bonsall, R. W., & Warner, P. (1974). Human vaginal secretions: Volatile fatty acid content. Science, 186(4170), 1217–1219.
Milton, K. (1985). Mating patterns of woolly spider monkeys, Brachyteles arachnoides: IImplications for female choice. Behavioral Ecology and Sociobiology, 17(1), 53–59.
Nakagawa, N. (1989). Bioenergetics of Japanese monkeys (Macaca fuscata) on Kinkazan Island during winter. Primates, 30(4), 441–460.
Nigi, H. (1975). Menstrual cycle and some other related aspects of Japanese monkeys (Macaca fuscata). Primates, 16(2), 207–216.
Nishimura, A., Fonseca, G., Mittermeier, R., Young, A., Strier, K. B., & Vall, C. (1988). The muriqui, genus Brachyteles. In R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho, & G. A. B. Fonseca (Eds.), Ecology and behavior of neotropical primates (Vol. 2, pp. 557–610). Washington, DC: World Wildlife Fund–US.
Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Animal Behaviour, 58(2), 229–246.
O’Neill, A. C., Fedigan, L. M., & Ziegler, T. E. (2004). Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata). American Journal of Physical Anthropology, 125(4), 352–362.
Parga, J. A. (2003). Copulatory plug displacement evidences sperm competition in Lemur catta. International Journal of Primatology, 24(4), 889–899.
Pfefferle, D., Brauch, K., Heistermann, M., Hodges, J. K., & Fischer, J. (2008). Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome. Proceedings of the Royal Society of London B: Biological Sciences, 275(1634), 571–578.
Phillips, K. A., Buzzell, C. A., Holder, N., & Sherwood, C. C. (2011). Why do capuchin monkeys urine wash? An experimental test of the sexual communication hypothesis using fMRI. American Journal of Primatology, 73(6), 578–584.
Pradhan, G. R., Engelhardt, A., van Schaik, C. P., & Maestripieri, D. (2006). The evolution of female copulation calls in primates: A review and a new model. Behavioral Ecology and Sociobiology, 59(3), 333–343.
Reynolds, R. L., & Van Horn, R. N. (1977). Induction of estrus in intact Lemur catta under photoinhibition of ovarian cycles. Physiology & Behavior, 18(4), 693–700.
Rigaill, L., Higham, J. P., Lee, P. C., Blin, A., & Garcia, C. (2013). Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis). American Journal of Primatology, 75(7), 774–787.
Rigaill, L., MacIntosh, A. J. J., Higham, J. P., Winters, S., Shimizu, K., et al (2015). Multimodal advertisement of pregnancy in free-ranging female Japanese macaques (Macaca fuscata). PloS One, 10(8), e0135127.
Schilling, A. (1979). Olfactory communication in prosimians. In G. A. Doyle & R. D. Martin (Eds.), The study of prosimian behavior (pp. 461–542). New York: Academic Press.
Setchell, J. M., Vaglio, S., Moggi-Cecchi, J., Boscaro, F., Calamai, L., & Knapp, L. A. (2010). Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): Influence of sex, male status, and individual identity. Chemical Senses, 35(3), 205–220.
Shideler, S. E., Lindburg, D. G., & Lasley, B. L. (1983). Estrogen-behavior correlates in the reproductive physiology and behavior of the ruffed lemur (Lemur variegatus). Hormones and Behavior, 17(3), 249–263.
Shimizu, K., Udono, T., Tanaka, C., Narushima, E., Yoshihara, M., et al (2003). Comparative study of urinary reproductive hormones in great apes. Primates, 44(2), 183–190.
Skaug, H. J., Fournier, D. A., Bolker, B., Magnusson, A., & Nielsen, A. (2014). Generalized linear mixed models using AD Model Builder. R package version 0.8.0.
Smith, T. (2006). Individual olfactory signatures in common marmosets (Callithrix jacchus). American Journal of Primatology, 68(6), 585–604.
Taussky, H. H. (1954). A microcolorimetric determination of creatine in urine by the Jaffe reaction. Journal of Biological Chemistry, 208(2), 853–862.
Ueno, Y. (1994). Responses to urine odor in the tufted capuchin (Cebus apella). Journal of Ethology, 12(2), 81–87.
Vaglio, S., Minicozzi, P., Romoli, R., Boscaro, F., Pieraccini, G., et al (2016). Sternal gland scent-marking signals sex, age, rank, and group identity in captive mandrills. Chemical Senses, 41(2), 177–186.
Voss, R. (1979). Male accessory glands and the evolution of copulatory plugs in rodents. Occasional Papers of the Museum of Zoology, University of Michigan, 1–27.
Acknowledgments
We thank the members of the Social Systems Section of the Primate Research Institute of Kyoto University for their help with the experiments. We thank Prof. Ikuma Adachi for helpful comments on the design of the study protocol. We also thank Prof. Phyllis Lee, Prof. Fred Bercovitch, Prof. Joanna Setchell, and two anonymous reviewers for their comments on the manuscript. This work was supported by the Centre National de la Recherche Scientifique (France), Projet International de Coopération Scientifique (grant number 06274, to C. Garcia), and the Japan Society for the Promotion of Science (to L. Rigaill).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Handling Editor: Joanna M. Setchell
Rights and permissions
About this article
Cite this article
Rigaill, L., Suda-Hashimoto, N., Ducroix, L. et al. Testing for Links Between Female Urine Odor and Male Sexual Behaviors in Japanese Macaques (Macaca fuscata). Int J Primatol 38, 823–837 (2017). https://doi.org/10.1007/s10764-017-9980-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-017-9980-y