Skip to main content
Log in

Signaling of Reproductive Status in Captive Female Golden-Headed Lion Tamarins (Leontopithecus chrysomelas)

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

In species in which paternal care has an important impact on the offspring's fitness, concealment of reproductive status has been proposed as a strategy employed by females to prevent males from practicing desertion and polygamy, which would then lead to monogamous or polyandrous mating systems or both. We investigated whether the female's reproductive status is being concealed in golden-headed lion tamarins, which exhibit extensive paternal care and a mainly monogamous/polyandrous mating system. We used a combination of behavioral observations and endocrine data to determine female reproductive status and to examine changes in sociosexual behaviors over the ovarian cycle and between conceptive and nonconceptive cycles. Females clearly signaled their reproductive status by way of proceptive sexual presenting. Males showed increased frequencies of anogenital sniffing and mounting during the fertile period, indicating that they detected changes in olfactory and behavioral cues emitted by females, and they adjusted their mounting behavior accordingly. Males and females also remained in closer proximity before and during the fertile period, which suggests the existence of mate guarding. We discuss a possible function of behavioral advertisement of reproductive status in shaping the mating system in Leontopithecus chrysomelas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  • Alexander, R. D., and Noonan, K. M. (1979). Concealment of ovulation, parental care and human social evolution. In Chagnon, N. A., and Irons, W. (eds.), Evolutionary Biology and Human Social Behavior. An Anthropological Perspective, Duxbury Press, North Sciutate, Massachusetts, pp. 436-453.

    Google Scholar 

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

    Google Scholar 

  • Austin, C. R. (1982). The egg. In Austin, C. R., and Short, R. (eds.), Reproduction in Mammals, Vol. 1., Cambridge University Press, Cambridge, pp. 46-62.

    Google Scholar 

  • Baker, R. R., and Bellis, M. A. (1995). Human Sperm Competition, Chapman and Hall, London.

    Google Scholar 

  • Baker, A. J., Dietz, J. M., and Kleiman, D. G. (1993). Behavioural evidence for monopolization of paternity in multi-male groups of golden-lion tamarins. Anim. Behav. 46: 1091-1103.

    Google Scholar 

  • Birkhead, T. R. (1998). Sperm competition in birds: Mechanisms and function. In Birkhead, T. R., and Moller, A. P. (eds.), Sperm Competition and Sexual Selection. Academic Press, San Diego, pp. 579-622.

    Google Scholar 

  • Brand, H. M., and Martin, R. D. (1983). The relationship between female urinary estrogen excretion and mating behavior in cotton-topped tamarins, Saguinus oedipus oedipus. Int. J. Primatol. 4(3): 275-290.

    Google Scholar 

  • Burt, A. (1992). 'Concealed ovulation' and sexual signals in primates. Folia Primatol. 58: 1-6.

    Google Scholar 

  • Christen, A. (1974). Fortpflanzungsbiologie und Verhalten bei Cebuella pygmaea und Tamarin tamarin. Z. Tierpsychol. (Suppl.) 14: 1-79.

    Google Scholar 

  • Converse, L. J., Carlson, A. A., Ziegler, T. E., and Snowdon, C. T. (1995). Communication of ovulatory state to mates by female pygmy marmosets, Cebuella pygmaea. Anim. Behav. 49: 615-621.

    Google Scholar 

  • Davies, N. B. (1991). Mating systems. In Krebs, J. R., and Davies, N. B. (eds.). Behavioural Ecology. An Evolutionary Approach, Blackwell, Oxford, pp. 263-294.

    Google Scholar 

  • Davies, N. B., Hatchwell, B. J., Robson, T., and Burke, T. (1992). Paternity and parental effort in dunnocks Prunella modularis: How good are male chick-feeding rules? Anim. Behav. 43: 729-745.

    Google Scholar 

  • Dietz, J. (1997). Report from the field: Golden-headed lion tamarins in Una. Tamarin Tales 1: 6.

    Google Scholar 

  • Dietz, J. M. N., De Sousa, S., and Billerbeck, R. (1996). Population dynamics of goldenheaded lion tamarins Leontopithecus chrysomelas in Una Reserve, Brazil. Dodo J. Wildl. Preserv. Trusts 32: 115-122.

    Google Scholar 

  • Digby, L. J. (1999). Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus). Folia Primatol. 70: 136-145.

    Google Scholar 

  • Dixson, A. F. (1993). Callitrichid mating systems: Laboratory and field approaches to studies of monogamy and polyandry. In Rylands, A. B. (ed.), Marmosets and Tamarins: Systematics, Behaviour and Ecology, Oxford University Press, Oxford, pp. 164-175.

    Google Scholar 

  • Dixson, A. F. (1998). Primate Sexuality: Comparative Studies of Prosimians, Monkeys, Apes and Human Beings, Oxford University Press, Oxford, pp. 358-376.

    Google Scholar 

  • Dixson, A. F., and Lunn, S. F. (1987). Post-partum changes in hormones and sexual behaviour in captive groups of marmosets (Callithrix jacchus). Physiol. Behav. 41(6): 577-583.

    Google Scholar 

  • Dukelow, W. R., Piesce, D. L., Roudebusch, W. E., Jarosz, S. J., and Sengoku, K. (1990). In vitro fertilization in nonhuman primates. J. Med. Primatol. 19: 627-639.

    Google Scholar 

  • Dunbar, R. I. M. (1995). The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim. Behav. 50: 1057-1070.

    Google Scholar 

  • Eastman, S. A. K., Makawiti, D. M., Collins, W. P., and Hodges, J. K. (1984). The pattern of excretion of urinary steroid metabolites during the ovarian cycle and pregnancy in the marmoset monkey. J. Endocrol. 102: 19-26.

    Google Scholar 

  • French, J. A. (1997). Proximate regulation of singular breeding in callitrichid primates. In Solomon, N. G., and French, J. A. (eds.), Cooperative Breeding in Mammals, Cambridge University Press, Cambridge, pp. 34-75.

    Google Scholar 

  • French, J. A., and Schaffner, C. M. (in press). Contextual influences on sociosexual behavior in monogamous primates. In Wallen, K., and Schneider, J. (eds.), Reproduction in Context, MIT Press, Cambridge, Massachusetts.

  • French, J. A., DeGraw, W. A., Hendricks, S. E., Wegner, F., and Bridson, W. E. (1992). Urinary and plasma gonadotropin concentrations in golden lion tamarins (Leontopithecus r. rosalia). Am. J. Primatol. 26: 53-59.

    Google Scholar 

  • Goldizen, A. W. (1987). Facultative polyandry and the role of infant-carrying in wild saddleback tamarins (Saguinus fuscicollis). Behav. Ecol. Sociobiol. 20: 99-109.

    Google Scholar 

  • Gomendio, M., Harcourt, A. H., and Roldán, E. R. S. (1998). Sperm competition in mammals. In Birkhead, T. R., and Moller, A. P. (eds.), Sperm Competition and Sexual Selection, Academic Press, San Diego, pp. 667-755.

    Google Scholar 

  • Gray, E. M. (1996). Female control of offspring paternity in a Western population of red-winged blackbirds (Agelaius phoeniceus). Behav. Ecol. Sociobiol. 38: 267-278.

    Google Scholar 

  • Heistermann, M., and Hodges, J. K. (1995). Endocrine monitoring of the ovarian cycle and pregnancy in the saddle-back tamarin (Saguinus fuscicollis) by measurement of steroid conjugates in urine. Am. J. Primatol. 35: 117-127.

    Google Scholar 

  • Heistermann, M., Möhle, U., Vervaecke, H., Van Elsacker, L., and Hodges, J. K. (1996). Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biol. Reprod. 55: 844-853.

    Google Scholar 

  • Hinde, R. A., and Atkinson, S. (1970). Assessing the roles of social partners in maintaining mutual proximity as exemplified by mother/infant relations in monkeys. Anim. Behav. 18: 169-176.

    Google Scholar 

  • Hoage, R. J. (1982). Social and physical maturation in captive lion tamarins, Leontopithecus rosalia rosalia (Primates, Callitrichidae). Smithson. Contrib. Zool. 354: 1-50.

    Google Scholar 

  • Hrdy, S. B., and Whitten, P. L. (1987). Patterning of sexual activity. In Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R., and Struhsaker, T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 370-384.

    Google Scholar 

  • Johnson, M., and Everitt, B. J. (1988). Essential Reproduction, 3rd ed., Blackwell, Oxford.

    Google Scholar 

  • Kempenaers, B., Verheyen, G. R., Van den Broeck, M., Burke, T., Van Broeckhoven, C., and Dhondt, A. A. (1992). Extra-pair paternity results from female preference for highquality males in the blue tit. Nature 357: 494-496.

    Google Scholar 

  • Kempenaers, B., Verheyen, G. R., and Dhondt, A. A. (1995). Mate guarding and copulation behaviour in monogamous and polygynous blue tits: Do males follow a best-of-a-bad-job strategy? Behav. Ecol. Sociobiol. 36: 33-42.

    Google Scholar 

  • Kendrick, K. M., and Dixson, A. F. (1983). The effect of the ovarian cycle on the sexual behaviour of the common marmoset (Callithrix jacchus). Physiol. Behav. 30(5): 735-742.

    Google Scholar 

  • Kleiman, D. G. (1977). Characteristics of reproduction and sociosexual interactions in pairs of lion tamarins (Leontopithecus rosalia) during the reproductive cycle. In Kleiman, D. G. (ed.), The Biology and Conservations of the Callitrichidae, Smithsonian Institution Press, Washington, D.C., pp. 181-190.

    Google Scholar 

  • Kleiman, D. G., and Mack, D. S. (1977). A peak in sexual activity during mid-pregnancy in the golden lion tamarin, Leontopithecus rosalia (Primates: Callitrichidae). J. Mammal. 58(4): 657-660.

    Google Scholar 

  • Kleiman, D. G., Hoage, R. J., and Green, K. M. (1988). The lion tamarins, genus Leontopithecus. In Mittermeier, R. A., Rylands, A. B., Coimbra-Filho, A., and Fonseca, G. A. B. (eds.), Ecology and Behavior of Neotropical Primates, Vol. 2, WWF, Washington D.C., pp. 299-347.

    Google Scholar 

  • Lumpkin, S. (1981). Avoidance of cuckoldry in birds: The role of the female. Anim. Behav. 29: 303-304.

    Google Scholar 

  • Mack, D. S., and Kleiman, D. G. (1978). Distribution of scent marks in different contexts in captive lion tamarins Leontopithecus rosalia (Primates). In Rothe, H., Wolters, H. J., and Hearn, J. P. (eds.), Biology and Behaviour of Marmosets, Eigenverlag, Göttingen, pp. 181-188.

    Google Scholar 

  • Monfort, S. L., Bush, M., and Wildt, D. E. (1996). Natural and induced ovarian synchrony in golden lion tamarins (Leontopithecus rosalia). Biol. Reprod. 55: 875-882.

    Google Scholar 

  • Pagel, M. (1994). The evolution of conspicuous oestrous advertisement in Old World Monkeys. Anim. Behav. 47: 1333-1341.

    Google Scholar 

  • Price, E. C. (1992). Sex and helping: Reproductive strategies of breeding male and female cotton-top tamarins, Saguinus oedipus. Anim. Behav. 43: 717-728.

    Google Scholar 

  • Rothe, H. (1975). Some aspects of sexuality and reproduction in groups of captive marmosets (Callithrix jacchus). Z. Tierpsychol. 37: 255-273.

    Google Scholar 

  • Savage, A., Giraldo, L. H., Soto, L. H., and Snowdon, C. T. (1996). Demography, group composition, and dispersal in wild cotton-top tamarin (Saguinus oedipus) groups. Am. J. Primatol. 38: 85-100.

    Google Scholar 

  • Sillèn-Tullberg, B., and Moller, A. P. (1993). The relationship between concealed ovulation and mating systems in anthropoid primates: A phylogenetic analysis. Am. Nat. 141(1): 1-25.

    Google Scholar 

  • Smith, R. L. (1984). Sperm Competition and the Evolution of Animal Mating Systems, Academic Press, London.

    Google Scholar 

  • Soini, P. (1987). Sociosexual behavior of a free-ranging Cebuella pygmaea (Callitrichidae, Platyrrhini) troop during postpartum estrus of its reproductive female. Am. J. Primatol. 13: 223-230.

    Google Scholar 

  • Sokal, R. R., and Rohlf, F. J. (1981). Biometry, 2nd ed., Freeman, New York.

    Google Scholar 

  • Stribley, J. A., French, J. A., and Inglett, B. J. (1987). Mating patterns in the golden lion tamarin (Leontopithecus rosalia): Continuous receptivity and concealed estrus. Folia Primatol. 49: 137-150.

    Google Scholar 

  • Sussman, R. W., and Garber, P. A. (1984). A new interpretation of the social organization and mating system of the Callitrichidae. Int. J. Primatol. 8(1): 73-92.

    Google Scholar 

  • Tardif, S. D. (1997). The bioenergetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. In Solomon, N. G., and French, J. A. (eds.), Cooperative Breeding in Mammals, Cambridge University Press, Cambridge, pp. 11-33.

    Google Scholar 

  • Terborgh, J., and Goldizen, A. W. (1985). On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis). Behav. Ecol. Sociobiol. 16: 293-299.

    Google Scholar 

  • Van Elsacker, L., Heistermann, M., Hodges, J. K., De Laet, A., and Verheyen, R. F. (1994). Preliminary results on the evaluation of contraceptive implants in golden-headed lion tamarins, Leontopithecus chrysomelas. Neotrop. Primates 2(Suppl.): 30-32.

    Google Scholar 

  • Vervaecke, H. (1999). Dominance relationships, bonding and the female genital swelling cycle in bonobos (Pan paniscus). Ph.D. dissertation, University of Antwerp, Belgium.

    Google Scholar 

  • Ziegler, T. E., Savage, A., Scheffler, G., and Snowdon, C. T. (1987). The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions. Biol. Reprod. 37: 618-627.

    Google Scholar 

  • Ziegler, T. E., Snowdon, C. T., and Bridson, W. E. (1990a). Reproductive performance and excretion of urinary estrogens and gonadotropins in the female pygmymarmoset (Cebuella pygmaea). Am. J. Primatol. 22: 191-203.

    Google Scholar 

  • Ziegler, T. E., Snowdon, C. T., Warneke, M., and Bridson, W. E. (1990b). Urinary excretion of oestrone conjugates and gonadotrophins during pregnancy in the Goeldi's monkey (Callimico goeldii). J. Reprod. Fertil. 89: 163-168.

    Google Scholar 

  • Ziegler, T. E., Wittwer, D. J., and Snowdon, C. T. (1993a). Circulating and excreted hormones during the ovarian cycle in the cotton-top tamarin, Saguinus oedipus. Am. J. Primatol. 31: 55-65.

    Google Scholar 

  • Ziegler, T. E., Epple, G., Snowdon, C. T., Porter, T. A., Belcher, A. M., and Küderling, I. (1993b). Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Anim. Behav. 45: 313-322.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Vleeschouwer, K., Heistermann, M., Van Elsacker, L. et al. Signaling of Reproductive Status in Captive Female Golden-Headed Lion Tamarins (Leontopithecus chrysomelas). International Journal of Primatology 21, 445–465 (2000). https://doi.org/10.1023/A:1005439919150

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005439919150

Navigation