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18 - Sexual Behavior in Marmosets in the Context of Cooperative Breeding

from Part III - Nonhuman Primate Sexual Behavior

Published online by Cambridge University Press:  30 June 2022

By
Aaryn C. Mustoe  and
Jeffrey A. French
Edited by
Todd K. Shackelford
Todd K. Shackelford
Affiliation:
Oakland University, Michigan
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Summary

Sexual behavior in marmosets (Callithrix spp.) occurs within the context of cooperative breeding, a social system characterized by biparental and alloparental infant care, family-like social demography, and features of social monogamy. Both male and female reproductive strategies and sexual behavior are influenced by the social features of cooperative breeding. In this chapter, we first review the fundamentals of copulatory behavior in marmosets and its coordination by visual and olfactory cues. We then discuss the intricacies of the definition of “social monogamy” in primates and address the degree to which the concept is applicable to marmosets.In captivity, the only stable group demography is a monogamous pairing of a single adult male and female and their offspring. This demography is common in free-ranging groups of marmosets in eastern Brazil, but groups with multiple breeding males and/or females have been reported, suggesting flexibility in the mating system in marmosets. Reproductive strategies in marmosets are complex, and include inhibition of sexual behavior and physiology in subordinates, extrapair copulation and mating with individuals from neighboring groups especially during territorial encounters, extensive infant care by males and older offspring, and the formation of strong social attachments between breeding males and females. We conclude this chapter with a discussion of the proximate role of sex steroids in regulating features of marmoset sexual behavior, and propose that the neurohormone oxytocin plays a large role in orchestrating the social strategies that contribute to the unique features of marmoset sociosexual behavior.

Keywords

marmosetsexual behaviormonogamypolyandrypolygynyreproductionoxytocin
Type
Chapter
Information
The Cambridge Handbook of Evolutionary Perspectives on Sexual Psychology , pp. 464 - 493
Publisher: Cambridge University Press
Print publication year: 2022

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References

Ågmo, A., Smith, A. S., Birnie, A. K., & French, J. A. (2012). Behavioral characteristics of pair bonding in the black tufted-ear marmoset (Callithrix penicillata). Behaviour, 149(3–4), 407–440.Google ScholarPubMed
Abbott, David H. (1993). Social conflict and reproductive suppression in marmoset and tamarin monkeys. In Mason, W. A. & Mendoza, S. P. (Eds.), Primate Social Conflict (pp. 331–372). Albany, NY: SUNY Press.Google Scholar
Abbott, D. H. (1984). Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. American Journal of Primatology, 6(3), 169–186.Google Scholar
Abbott, David H., Saltzman, W., Schultz-Darken, N. J., & Smith, T. E. (1997). Specific neuroendocrine mechanisms not involving generalized stress mediate social regulation of female reproduction in cooperatively breeding marmoset monkeys. Annals of the New York Academy of Sciences, 807(1), 219–238.Google Scholar
Abreu, F., De la Fuente, M. F. C., Schiel, N., & Souto, A. (2016). Feeding ecology and behavioral adjustments: Flexibility of a small neotropical primate (Callithrix jacchus) to survive in a semiarid environment. Mammal Research, 61(3), 221–229.Google Scholar
Albuquerque, A. C. S., Sousa, M. B., Santos, H. M., & Ziegler, T. E. (2001). Behavioral and hormonal analysis of social relationships between oldest females in a wild monogamous group of common marmosets (Callithrix jacchus). International Journal of Primatology, 22(4), 631–645.Google Scholar
Alonso, C., & Langguth, A. (1989). Ecology and behavior of Callithrix jacchus (Primates: Callitrichidae) living on an Atlantic forest island. Revista Nordestina de Biologia, 6, 105–137.Google Scholar
Anzenberger, G. (1985). How stranger encounters of common marmosets (Callithrix jacchus jacchus) are influenced by family members: The quality of behavior. Folia Primatologica, 45(3–4), 204–224.Google Scholar
Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience & Biobehavioral Reviews, 30(3), 319–345.Google Scholar
Arruda, M. F., Araújo, A., Sousa, M. B. C., Albuquerque, F. S., Albuquerque, A. C. S. R., & Yamamoto, M. E. (2005). Two breeding females within free-living groups may not always indicate polygyny: Alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatologica: International Journal of Primatology, 76(1), 10–20.Google Scholar
Barrett, J., Abbott, D. H., & George, L. M. (1990). Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. Reproduction, 90(2), 411–418.Google Scholar
Blaustein, J. D., & McCarthy, M. M. (2009). Phoenix, Goy, Gerall, and Young, Endocrinology, 1959: 50 years young and going strong. Endocrinology, 150(6), 2501–2501.Google Scholar
Burkart, J. M. (2015). Opposite effects of male and female helpers on social tolerance and proactive prosociality in callitrichid family groups. Scientific Reports, 5(1), 1–9.CrossRefGoogle ScholarPubMed
Burkart, J. M., Fehr, E., Efferson, C., & van Schaik, C. P. (2007). Other-regarding preferences in a non-human primate: Common marmosets provision food altruistically. Proceedings of the National Academy of Sciences, 104(50), 19762–19766.CrossRefGoogle Scholar
Burkart, J. M., Hrdy, S. B., & Van Schaik, C. P. (2009). Cooperative breeding and human cognitive evolution. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews, 18(5), 175–186.Google Scholar
Burkart, J. M., & van Schaik, C. P. (2016). Revisiting the consequences of cooperative breeding. Journal of Zoology, 299(2), 77–83.Google Scholar
Campbell, S. K., & Cortés-Ortiz, L. (2021). Oxytocin amino acid variation within Neotropical primates: New genetic variants in hormone and receptor sequences and evidence for evolutionary forces driving this unexpected diversity. Biological Journal of the Linnean Society, 132(1), 211–220.CrossRefGoogle Scholar
Carp, S. B., Rothwell, E. S., Bourdon, A., Freeman, S. M., Ferrer, E., & Bales, K. L. (2016). Development of a partner preference test that differentiates between established pair bonds and other relationships in socially monogamous titi monkeys (Callicebus cupreus). American Journal of Primatology, 78(3), 326–339.CrossRefGoogle ScholarPubMed
Carp, S. B., Taylor, J. H., & French, J. A. (2019). Dopamine receptor manipulation does not alter patterns of partner preference in long-term marmoset pairs. Physiology & Behavior, 204, 290–296.CrossRefGoogle Scholar
Carter, C. S., & Perkeybile, A. M. (2018). The monogamy paradox: What do love and sex have to do with it? Frontiers in Ecology and Evolution, 6, 202.CrossRefGoogle Scholar
Cavanaugh, J., Carp, S. B., Rock, C. M., & French, J. A. (2016). Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys. Psychoneuroendocrinology, 66, 22–30.CrossRefGoogle ScholarPubMed
Cavanaugh, J., & French, J. A. (2013). Post-partum variation in the expression of paternal care is unrelated to urinary steroid metabolites in marmoset fathers. Hormones and Behavior, 63(4), 551–558.CrossRefGoogle ScholarPubMed
Cavanaugh, J., Huffman, M. C., Harnisch, A. M., & French, J. A. (2015). Marmosets treated with oxytocin are more socially attractive to their long-term mate. Frontiers in Behavioral Neuroscience, 9, 251.CrossRefGoogle ScholarPubMed
Cavanaugh, J., Mustoe, A., & French, J. A. (2018). Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets. American Journal of Primatology, 80(10), e22750.Google Scholar
Cavanaugh, J., Mustoe, A. C., Taylor, J. H., & French, J. A. (2014). Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers. Psychoneuroendocrinology, 49, 1–10.Google Scholar
Cavanaugh, J., Mustoe, A., Womack, S. L., & French, J. A. (2018). Oxytocin modulates mate-guarding behavior in marmoset monkeys. Hormones and Behavior, 106, 150–161.Google Scholar
Cavigelli, S. A., & Pereira, M. E. (2000). Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Hormones and Behavior, 37(3), 246–255.Google Scholar
Creel, S., Wildt, D. E., & Monfort, S. L. (1993). Aggression, reproduction, and androgens in wild dwarf mongooses: A test of the challenge hypothesis. The American Naturalist, 141(5), 816–825.CrossRefGoogle ScholarPubMed
da Silva Mota, M. T., Franci, C. R., & de Sousa, M. B. (2006). Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus). Hormones and Behavior, 49(3), 293–302.CrossRefGoogle ScholarPubMed
de Sousa, M. B. C., da Rocha Albuquerque, A. C. S., Yamamoto, M. E., Araújo, A., & de Fátima Arruda, M. (2009). Emigration as a reproductive strategy of the common marmoset (Callithrix jacchus). In Ford, S. M., Porter, L. M., & Davis, L. C. (Eds.), The smallest anthropoids (pp. 167–182). New York: Springer.Google Scholar
Digby, L. J. (1999). Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus). Folia Primatologica; International Journal of Primatology, 70(3), 136–145.Google Scholar
Digby, L. J. (1995). Social organization in a wild population of Callithrix jacchus: II. Intragroup social behavior. Primates, 36(3), 361–375.CrossRefGoogle Scholar
Digby, L. J., & Barreto, C. E. (1993). Social organization in a wild population of Callithrix jacchus. Folia Primatologica, 61(3), 123–134.CrossRefGoogle Scholar
Dixson, A. F. (1986). Proceptive displays of the female common marmoset (Callithrix jacchus): Effects of ovariectomy and oestradiol 17 beta. Physiology & Behavior, 36(5), 971–973.Google Scholar
Dixson, A. F. (1990). Medial hypothalamic lesions and sexual receptivity in the female common marmoset (Callithrix jacchus). Folia Primatologica: International Journal of Primatology, 54(1–2), 46–56.CrossRefGoogle ScholarPubMed
Dixson, A. F. (1993a). Effects of testosterone propionate upon the sexual and aggressive behavior of adult male marmosets (Callithrix jacchus) castrated as neonates. Hormones and Behavior, 27(2), 216–230.CrossRefGoogle ScholarPubMed
Dixson, A. F. (1993b). Sexual and aggressive behaviour of adult male marmosets (Callithrix jacchus) castrated neonatally, prepubertally, or in adulthood. Physiology & Behavior, 54(2), 301–307.CrossRefGoogle ScholarPubMed
Dixson, A. (2001). The evolution of neuroendocrine mechanisms regulating sexual behaviour in female primates. Reproduction, Fertility, and Development, 13(7–8), 599–607.Google Scholar
Dixson, A. F., & Lunn, S. F. (1987). Post-partum changes in hormones and sexual behaviour in captive groups of marmosets (Callithrix jacchus). Physiology & Behavior, 41(6), 577–583.Google Scholar
Epple, G. (1993). Making sense out of scents: Species differences in scent glands, scent-marking behavior, and scent-marking composition in Callitrichidae. In Rylands, A. B. (Ed.), Marmosets and tamarins: Systematics, behavior, and ecology (pp. 123–151). Oxford: Oxford University Press.Google Scholar
Erb, W. M., & Porter, L. M. (2017). Mother’s little helpers: What we know (and don’t know) about cooperative infant care in callitrichines. Evolutionary Anthropology: Issues, News, and Reviews, 26(1), 25–37.Google Scholar
Evans, S. (1983). The pair-bond of the common marmoset, Callithrix jacchus: An experimental investigation. Animal Behaviour, 31(3), 651–658.Google Scholar
Faulkes, C. G., Arruda, M. F., & Monteiro da Cruz, M. A. O. (2003). Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset, Callithrix jacchus. Molecular Ecology, 12(4), 1101–1108.CrossRefGoogle ScholarPubMed
Fernandez-Duque, E., Huck, M., Van Belle, S., & Di Fiore, A. (2020). The evolution of pair-living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins. American Journal of Physical Anthropology, 171, 118–173.CrossRefGoogle ScholarPubMed
Ferrari, S. F. (1992). The care of infants in a wild marmoset (Callithrix flaviceps) group. American Journal of Primatology, 26(2), 109–118.Google Scholar
Ferrari, S. F., & Ferrari, M. A. L. (1989). A re-evaluation of the social organisation of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatologica, 52(3–4), 132–147.CrossRefGoogle Scholar
Ferris, C. F., Snowdon, C. T., King, J. A., Duong, T. Q., Ziegler, T. E., Ugurbil, K., … & Vaughan, J. T. (2001). Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues. Neuroreport, 12(10), 2231–2236.Google Scholar
Ferris, C. F., Snowdon, C. T., King, J. A., Sullivan, J. M., Ziegler, T. E., Olson, D. P., … & Duong, T. Q. (2004). Activation of neural pathways associated with sexual arousal in non-human primates. Journal of Magnetic Resonance Imaging, 19(2), 168–175.Google Scholar
Finkenwirth, C., & Burkart, J. M. (2017). Long-term-stability of relationship structure in family groups of common marmosets, and its link to proactive prosociality. Physiology & Behavior, 173, 79–86.Google Scholar
Finkenwirth, C., Martins, E., Deschner, T., & Burkart, J. M. (2016). Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys. Hormones and Behavior, 80, 10–18.Google Scholar
Finkenwirth, C., van Schaik, C., Ziegler, T. E., & Burkart, J. M. (2015). Strongly bonded family members in common marmosets show synchronized fluctuations in oxytocin. Physiology & Behavior, 151, 246–251.Google Scholar
Fite, J. E., Patera, K. J., French, J. A., Rukstalis, M., Hopkins, E. C., & Ross, C. N. (2005). Opportunistic mothers: Female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can. Journal of Human Evolution, 49(1), 122–142.Google Scholar
French, J. A. (1997). Regulation of singular breeding in callitrichid primates. In Solomon, N. G. & French, J. A. (Eds.), Cooperative breeding in mammals (pp. 34–75). Cambridge: Cambridge University Press.Google Scholar
French, J. A., Cavanaugh, J., Mustoe, A. C., Carp, S. B., & Womack, S. L. (2018). Social monogamy in nonhuman primates: Phylogeny, phenotype, and physiology. The Journal of Sex Research, 55(4–5), 410–434.Google Scholar
French, J. A., Mustoe, A. C., Cavanaugh, J., & Birnie, A. K. (2013). The influence of androgenic steroid hormones on female aggression in “atypical” mammals. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1631), 20130084.Google Scholar
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016). Neuropeptide diversity and the regulation of social behavior in New World primates. Frontiers in Neuroendocrinology, 42, 18–39.CrossRefGoogle ScholarPubMed
Garber, P. A. (1992). Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. American Journal of Physical Anthropology, 88(4), 469–482.Google Scholar
Garbino, G. S., & Martins-Junior, A. M. (2018). Phenotypic evolution in marmoset and tamarin monkeys (Cebidae, Callitrichinae) and a revised genus-level classification. Molecular Phylogenetics and Evolution, 118, 156–171.Google Scholar
Gibson, K. N. (2010). Male mating tactics in spider monkeys: Sneaking to compete. American Journal of Primatology, 72(9), 794–804.Google Scholar
Goldizen, A. W. (1990). A comparative perspective on the evolution of tamarin and marmoset social systems. International Journal of Primatology, 11(1), 63–83.Google Scholar
Hubrecht, R. C. (1985). Home-range size and use and territorial behavior in the common marmoset, Callithrix jacchus, at the Tapacura Field Station, Recife, Brazil. International Journal of Primatology, 6(5), 533–550.CrossRefGoogle Scholar
Johnson, E. O., Kamilaris, T. C., Carter, S., Gold, P. W., & Chrousos, G. P. (1991). Environmental stress and reproductive success in the common marmoset (Callithrix jacchus jacchus). American Journal of Primatology, 25(3), 191–201.CrossRefGoogle ScholarPubMed
Jurek, B., & Neumann, I. D. (2018). The oxytocin receptor: From intracellular signaling to behavior. Physiological Reviews, 98(3), 1805–1908.Google Scholar
Kappeler, P. M., & Pozzi, L. (2019). Evolutionary transitions toward pair living in nonhuman primates as stepping stones toward more complex societies. Science Advances, 5(12), eaay1276.Google Scholar
Kendrick, K. M., & Dixson, A. F. (1983). The effect of the ovarian cycle on the sexual behaviour of the common marmoset (Callithrix jacchus). Physiology & Behavior, 30(5), 735–742.Google Scholar
Kendrick, K. M., & Dixson, A. F. (1984). A quantitative description of copulatory and associated behaviors of captive marmosets (Callithrix jacchus). International Journal of Primatology, 5(3), 199–212.Google Scholar
Kendrick, K. M., & Dixson, A. F. (1985). Effects of oestradiol 17B, progesterone and testosterone upon proceptivity and receptivity in ovariectomized common marmosets (Callithrix jacchus). Physiology & Behavior, 34(1), 123–128.CrossRefGoogle ScholarPubMed
Kotani, M., Shimono, K., Yoneyama, T., Nakako, T., Matsumoto, K., Ogi, Y., Konoike, N., Nakamura, K., & Ikeda, K. (2017). An eye tracking system for monitoring face scanning patterns reveals the enhancing effect of oxytocin on eye contact in common marmosets. Psychoneuroendocrinology, 83, 42–48.Google Scholar
Kraynak, M., Colman, R. J., Flowers, M. T., Abbott, D. H., & Levine, J. E. (2019 ). Ovarian estradiol supports sexual behavior but not energy homeostasis in female marmoset monkeys. International Journal of Obesity, 43(5), 1034–1045.Google Scholar
Kuzawa, C. W., Gettler, L. T., Muller, M. N., McDade, T. W., & Feranil, A. B. (2009). Fatherhood, pairbonding and testosterone in the Philippines. Hormones and Behavior, 56(4), 429–435.CrossRefGoogle ScholarPubMed
la Fuente, D., Castellón, M. F., Souto, A., Sampaio, M. B., & Schiel, N. (2014). Behavioral adjustments by a small Neotropical primate (Callithrix jacchus) in a semiarid Caatinga environment. The Scientific World Journal. https://doi.org/10.1155/2014/326524CrossRefGoogle Scholar
Lazaro-Perea, C. (2001). Intergroup interactions in wild common marmosets, Callithrix jacchus: Territorial defence and assessment of neighbours. Animal Behaviour, 62(1), 11–21.Google Scholar
Lazaro-Perea, C., Castro, C. S., Harrison, R., Araujo, A., Arruda, M. F., & Snowdon, C. T. (2000). Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets. Behavioral Ecology and Sociobiology, 48(2), 137–146.Google Scholar
Lazaro-Perea, C., de Fátima Arruda, M., & Snowdon, C. T. (2004). Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets. Animal Behaviour, 67(4), 627–636.Google Scholar
Lazaro-Perea, C., Snowdon, C. T., & de Fátima Arruda, M. (1999). Scent-marking behavior in wild groups of common marmosets (Callithrix jacchus). Behavioral Ecology and Sociobiology, 46(5), 313–324.Google Scholar
Lee, A. G., Cool, D. R., Grunwald, W. C. Jr., Neal, D. E., Buckmaster, C. L., Cheng, M., … & Parker, K. J. (2011). A novel form of oxytocin in New World monkeys. Biology Letters, 7(4), 584–587.Google Scholar
Lloyd, S. A., & Dixson, A. F. (1988). Effects of hypothalamic lesions upon the sexual and social behaviour of the male common marmoset (Callithrix jacchus). Brain Research, 463(2), 317–329.CrossRefGoogle ScholarPubMed
Lúcio Nogueira, S., Cordeiro de Sousa, M. B., de Medeiros Neto, C. F., & da Paz de Oliveira Costa, M. (2001). Diurnal variation in scent marking behavior in captive male and female common marmosets, Callithrix jacchus. Biological Rhythm Research, 32(2), 169–177.CrossRefGoogle Scholar
Lukas, D., & Clutton-Brock, T. H. (2013). The evolution of social monogamy in mammals. Science, 341(6145), 526–530.Google Scholar
Lunn, S. F., & McNeilly, A. S. (1982). Failure of lactation to have a consistent effect on interbirth interval in the common marmoset, Callithrix jacchus jacchus. Folia Primatologica, 37(1–2), 99–105.Google Scholar
Lunn, S. F., Recio, R., Morris, K., & Fraser, H. M. (1994). Blockade of the neonatal rise in testosterone by a gonadotrophin-releasing hormone antagonist: Effects on timing of puberty and sexual behaviour in the male marmoset monkey. Journal of Endocrinology, 141(3), 439–447.Google Scholar
Michels, A. M. (1998). Sex differences in food acquisition and aggression in captive common marmosets (Callithrix jacchus). Primates, 39(4), 549.Google Scholar
Mustoe, A. C., Cavanaugh, J., Harnisch, A. M., Thompson, B. E., & French, J. A. (2015). Do marmosets care to share? Oxytocin treatment reduces prosocial behavior toward strangers. Hormones and Behavior, 71, 83–90.Google Scholar
Mustoe, A. C., Harnisch, A. M., Hochfelder, B., Cavanaugh, J., & French, J. A. (2016). Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin. Animal Behaviour, 114, 69–79.Google Scholar
Mustoe, A., Schulte, N. A., Taylor, J. H., French, J. A., & Toews, M. L. (2019). Leu 8 and Pro 8 oxytocin agonism differs across human, macaque, and marmoset vasopressin 1a receptors. Scientific Reports, 9(1), 1–10.Google Scholar
Mustoe, A., Taylor, J. H., & French, J. A. (2018). Oxytocin structure and function in New World monkeys: From pharmacology to behavior. Integrative Zoology, 13(6), 634–654.Google Scholar
Nievergelt, C. M., Digby, L. J., Ramakrishnan, U., & Woodruff, D. S. (2000). Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. International Journal of Primatology, 21(1), 1–20.Google Scholar
Nunes, S., Fite, J. E., Patera, K. J., & French, J. A. (2001). Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Hormones and Behavior, 39(1), 70–82.Google Scholar
Overduin-de Vries, A. M., Massen, J. J. M., Spruijt, B. M., & Sterck, E. H. M. (2012). Sneaky monkeys: An audience effect of male rhesus macaques (Macaca mulatta) on sexual behavior. American Journal of Primatology, 74(3), 217–228.Google Scholar
Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65(3), 369–382.Google Scholar
Price, E. C. (1990). Infant carrying as a courtship strategy of breeding male cotton-top tamarins. Animal Behaviour, 40(4), 784–786.Google Scholar
Ren, D., Lu, G., Moriyama, H., Mustoe, A. C., Harrison, E. B., & French, J. A. (2015). Genetic diversity in oxytocin ligands and receptors in New World monkeys. PLOS ONE, 10(5), e0125775.CrossRefGoogle ScholarPubMed
Ross, C. N., & French, J. A. (2011). Female marmosets’ behavioral and hormonal responses to unfamiliar intruders. American Journal of Primatology, 73(10), 1072–1081.Google Scholar
Ross, C. N., French, J. A., & Patera, K. J. (2004). Intensity of aggressive interactions modulates testosterone in male marmosets. Physiology & Behavior, 83(3), 437–445.CrossRefGoogle ScholarPubMed
Rothe, H. (1975). Some aspects of sexuality and reproduction in groups of captive marmosets (Callitbrix jacchus). Zeitschrift Fur Tierpsychologie, 37(3), 255–273.Google Scholar
Rukstalis, M., & French, J. A. (2005). Vocal buffering of the stress response: Exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Hormones and Behavior, 47(1), 1–7.Google Scholar
Saito, A., & Nakamura, K. (2011). Oxytocin changes primate paternal tolerance to offspring in food transfer. Journal of Comparative Physiology A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 197(4), 329–337.Google Scholar
Saltzman, W., Liedl, K. J., Salper, O. J., Pick, R. R., & Abbott, D. H. (2008). Post-conception reproductive competition in cooperatively breeding common marmosets. Hormones and Behavior, 53(1), 274–286.Google Scholar
Saltzman, W., Schultz Darken, N. J., & Abbott, D. H. (1997). Familial influences on ovulatory function in common marmosets (Callithrix jacchus). American Journal of Primatology, 41(3), 159–177.Google Scholar
Scanlon, C. E., Chalmers, N. R., & Da Cruz, M. M. (1988). Changes in the size, composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in north east Brazil. Primates, 29(3), 295–305.Google Scholar
Schaffner, C. M., Shepherd, R. E., Santos, C. V., & French, J. A. (1995). Development of heterosexual relationships in Wied’s black tufted ear marmosets (Callithrix kuhli). American Journal of Primatology, 36(3), 185–200.CrossRefGoogle ScholarPubMed
Schiel, N., & Huber, L. (2006). Social influences on the development of foraging behavior in free-living common marmosets (Callithrix jacchus). American Journal of Primatology, 68(12), 1150–1160.Google Scholar
Schiel, N., & Souto, A. (2017). The common marmoset: An overview of its natural history, ecology and behavior. Developmental Neurobiology, 77(3), 244–262.Google Scholar
Smith, A. S., Agmo, A., Birnie, A. K., & French, J. A. (2010). Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata. Hormones and Behavior, 57(2), 255–262.Google Scholar
Smith, T. E., & Abbott, D. H. (1998). Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus). American Journal of Primatology, 46(4), 265–284.Google Scholar
Smith, T. E., McGreer-Whitworth, B., & French, J. A. (1998). Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (Callithrix kuhli). Hormones and Behavior, 34(3), 211–222.Google Scholar
Snowdon, C. T. (1996). Infant care in cooperatively breeding species. Advances in the Study of Behavior, 25, 643–689.Google Scholar
Snowdon, C. T., Tannenbaum, P. L., Schultz-Darken, N. J., Ziegler, T. E., & Ferris, C. F. (2011). Conditioned sexual arousal in a nonhuman primate. Hormones and Behavior, 59(5), 696–701.Google Scholar
Snowdon, C. T., & Ziegler, T. E. (2007). Growing up cooperatively: Family processes and infant care in marmosets and tamarins. Journal of Developmental Processes, 2(1), 40–66.Google Scholar
Sousa, M. B. C., Albuquerque, A. C. S. da R., Albuquerque, F. da S., Araujo, A., Yamamoto, M. E., & Arruda, M. de F. (2005). Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups. American Journal of Primatology, 67(1), 37–50.CrossRefGoogle ScholarPubMed
Stevenson, M. F., & Poole, T. B. (1976). An ethogram of the common marmoset (Calithrix jacchus jacchus): General behavioural repertoire. Animal Behaviour, 24(2), 428–451.CrossRefGoogle ScholarPubMed
Sutcliffe, A. G., & Poole, T. B. (1978). Scent marking and associated behaviour in captive common marmosets (Callithrix jacchus jacchus) with a description of the histology of scent glands. Journal of Zoology, 185(1), 41–56.Google Scholar
Taniguchi, K., Matsusaki, Y., Ogawa, K., & Saito, T. R. (1992). Fine structure of the vomeronasal organ in the common marmoset (Callithrix jacchus). Folia Primatologica, 59(3), 169–176.Google Scholar
Tardif, S. D., & Bales, K. (1997). Is infant-carrying a courtship strategy in callitrichid primates? Animal Behaviour, 53(5), 1001–1007.Google Scholar
Tardif, S. D., Carson, R. L., & Gangaware, B. L. (1986). Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus). American Journal of Primatology, 11(2), 103–110.CrossRefGoogle ScholarPubMed
Tardif, S. D., Smucny, D. A., Abbott, D. H., Mansfield, K., Schultz-Darken, N., & Yamamoto, M. E. (2003). Reproduction in captive common marmosets (Callithrix jacchus). Comparative Medicine, 53(4), 364–368.Google Scholar
Taylor, J. H., Carp, S. B., & French, J. A. (2020). Vasopressin, but not oxytocin, modulates responses to infant stimuli in marmosets providing care to dependent infants. Developmental Psychobiology, 62(7), 932–940.CrossRefGoogle Scholar
Taylor, J. H., & French, J. A. (2015). Oxytocin and vasopressin enhance responsiveness to infant stimuli in adult marmosets. Hormones and Behavior, 75, 154–159.Google Scholar
Taylor, J. H., Intorre, A. A., & French, J. A. (2017). Vasopressin and oxytocin reduce food sharing behavior in male, but not female marmosets in family groups. Frontiers in Endocrinology, 8, 181.Google Scholar
Tecot, S. R., Singletary, B., & Eadie, E. (2016). Why “monogamy” isn’t good enough. American Journal of Primatology, 78(3), 340–354.Google Scholar
Thompson, C. L., Bottenberg, K. N., Lantz, A. W., de Oliveira, M. A., Melo, L. C., & Vinyard, C. J. (2020). What smells? Developing in-field methods to characterize the chemical composition of wild mammalian scent cues. Ecology and Evolution. https://doi.org/10.1002/ece3.6224Google Scholar
Vargas-Pinilla, P., Paixão-Côrtes, V. R., Paré, P., Tovo-Rodrigues, L., Vieira, C. M., Xavier, A., … & Bortolini, M. C. (2015). Evolutionary pattern in the OXT-OXTR system in primates: Coevolution and positive selection footprints. Proceedings of the National Academy of Sciences, 112(1), 88–93.Google Scholar
Wallen, K. (2001). Sex and context: Hormones and primate sexual motivation. Hormones and Behavior, 40(2), 339–357.CrossRefGoogle ScholarPubMed
Wallis, M. (2012). Molecular evolution of the neurohypophysial hormone precursors in mammals: Comparative genomics reveals novel mammalian oxytocin and vasopressin analogues. General and Comparative Endocrinology, 179(2), 313–318.Google Scholar
Wingfield, J. C., Ball, G. F., Dufty, A. M., Hegner, R. E., & Ramenofsky, M. (1987). Testosterone and aggression in birds. American Scientist, 75(6), 602–608.Google Scholar
Wingfield, J. C., Goymann, W., Jalabert, C., & Soma, K. K. (2020). Reprint of “Concepts derived from the Challenge Hypothesis.” Hormones and Behavior, 115, 104802.Google Scholar
Wingfield, J. C., Hegner, R. E., Dufty, A. M. Jr., & Ball, G. F. (1990). The “Challenge Hypothesis”: Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist, 136(6), 829–846.Google Scholar
Wislocki, G. B. (1930). A study of scent glands in the marmosets, especially Oedipomidas geoffroyi. Journal of Mammalogy, 11(4), 475–483.Google Scholar
Woodcock, A. J. (1982). The first weeks of cohabitation of newly-formed heterosexual pairs of common marmosets (Callithrix jacchus). Folia Primatologica; International Journal of Primatology, 37(3–4), 228–254.Google Scholar
Yamamoto, M. E. (2003). From dependence to sexual maturity: The behavioural ontogeny of Callitrichidae. In Rylands, A. B. (Ed.), Marmosets and tamarins: Systematics, behaviour and ecology. (pp. 235–250). Oxford: Oxford University Press.Google Scholar
Yamamoto, M. E., de Fátima Arruda, M., Alencar, A. I., de Sousa, M. B. C., & Araújo, A. (2009). Mating systems and female–female competition in the common marmoset, Callithrix jacchus. In Ford, S. M., Porter, L. M., & Davis, L. C., The smallest anthropoids (pp. 119–133). New York: Springer.Google Scholar
Young, L. J., & Wang, Z. (2004). The neurobiology of pair bonding. Nature Neuroscience, 7(10), 1048–1054.Google Scholar
Ziegler, T. E., Prudom, S. L., & Zahed, S. R. (2009). Variations in male parenting behavior and physiology in the common marmoset. American Journal of Human Biology, 21(6), 739–744.Google Scholar
Ziegler, T. E., Schultz-Darken, N. J., Scott, J. J., Snowdon, C. T., & Ferris, C. F. (2005). Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus. Hormones and Behavior, 47(1), 56–64.Google Scholar

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