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Endocrine Correlates of Reproductive Status in Breeding and Nonbreeding Wild Female Moustached Tamarins

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Abstract

In callitrichid primates, reproduction is usually restricted to a single female per group. Reproductive rate is high and the occurrence of a postpartum estrus can lead to simultaneous lactation and pregnancy. In contrast, nonreproductive females often show ovarian inactivity. However, most studies on callitrichid reproductive physiology have been conducted in captivity, where conditions differ considerably from those in the wild, so that reproductive conditions may be strongly modified. Using fecal estrogen and progestogen measurements to monitor female reproductive status in 2 groups of wild moustached tamarins (Saguinus mystax), we examined 1) whether reproductive females in free-ranging groups also show postpartum estrus and 2) whether nonreproductive females demonstrate signs of ovarian activity. In both reproductive females, clear changes in the excretion pattern of progestogen and estrogen metabolites over time in combination with information on parturition dates allowed us to differentiate between pregnancy, a period of postpartum ovarian inactivity lasting for 54 and 64–82 days, and a period of ovarian activity before conception. Nonreproductive females demonstrated temporal fluctuations in hormone concentrations and absolute hormone levels that were similar to ones in the breeding females during the phase of ovarian activity. The results suggest that, in contrast to most captive female tamarins, reproductive females in wild groups of moustached tamarins do not have a postpartum estrus and that nonreproductive females show ovarian activity despite the presence of a breeding female. We therefore conclude that findings from captivity should be only carefully compared to the situation in the wild.

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REFERENCES

  • Abbott, D. H. (1991) The social control of fertility. In Box, H. O. (ed.), Primate Responses to Environmental Change, Chapman and Hall, London, pp. 75-89.

    Google Scholar 

  • Abbott, D. H., Barrett, J., and George, L. M. (1993) Comparative aspects of the social suppression of reproduction in female marmosets and tamarins. In Rylands, A. B. (ed.), Marmosets and Tamarins—Systematics, Behaviour, and Ecology, Oxford Science Publications, Oxford, pp. 152-163.

    Google Scholar 

  • Abbott, D. H., and Hearn, J. P. (1978) Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey, Callithrix jacchus. J. Reprod. Fertil. 53: 155-166.

    Google Scholar 

  • Achenbach, G. G., and Snowdon, C. T. (2002) Costs of caregiving: Weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. Int. J. Primatol. 23(1): 179-189.

    Google Scholar 

  • Albuquerque, A. C. S. R., Sousa, M. B. C., Santos, H. M., and Ziegler, T. E. (2001) Behavioral and hormonal analysis of social relationships between oldest females in a wild monogamous group of common marmosets (Callitrix jacchus).Int. J. Primatol. 22(4): 631-645.

    Google Scholar 

  • Andersson, M. (1994) Sexual Selection, Princeton University Press, Princeton.

    Google Scholar 

  • Birkhead, T., and Møller, A. P. (1998) Sperm Competition and Sexual Selection, Academic Press, San Diego.

    Google Scholar 

  • Caine, N. G. (1993) Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour: The role of predation pressures. In Rylands, A. B. (ed.), Marmosets and Tamarins—Systematics, Behaviour, and Ecology, Oxford Science Publications, Oxford, pp. 200-219.

    Google Scholar 

  • Cordeiro de Sousa, M. B., Nascimento Lopes, M. C., and Albuquerque, A. C. S. R. (2002) Fecal collection in free-ranging common marmosets, Callithrix jacchus. Neotrop. Primates 10(1): 21-24.

    Google Scholar 

  • Curtis, D. J., Zaramody, A., Green, D. I., and Pickard, A. R. (2000) Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz).Reprod. Fertil. Dev. 12: 21-29.

    Google Scholar 

  • Digby, L. (1995) Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus).Behav. Ecol. Sociobiol. 37: 51-61.

    Google Scholar 

  • Dixson, A. F. (1983) Observations on the evolution and behavioral significance of “sexual skin” in female primates. Adv. Stud. Behav. 13: 63-106.

    Google Scholar 

  • Dixson, A. F. (1998) Primate Sexuality, Oxford University Press, Oxford.

    Google Scholar 

  • Eisenberg, J. F. (1977) Comparative ecology and reproduction of New World monkeys. In Kleiman, D. G. (ed.), The Biology and Conservation of the Callitrichidae, Smithsonian Institution, Washington, DC, pp. 13-22.

    Google Scholar 

  • Epple, G., and Katz, Y. (1984) Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis).Am. J. Primatol. 6: 215-227.

    Google Scholar 

  • Evans, S., and Hodges, J. K. (1984) Reproductive status of adult daughters in family groups of common marmosets (Callithrix jacchus jacchus).Folia Primatol. 42: 127-133.

    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., Abbott, D. H., and Snowdon, C. T. (1984) The effect of social environment on estrogen excretion, scent marking, and sociosexual behavior in tamarins (Saguinus oedipus).Am. J. Primatol. 6: 155-167.

    Google Scholar 

  • French, J. A., Bales, K. L., Baker, A. J., and Dietz, J. M. (2003) Endocrine monitoring of wild dominant and subordinate female Leontopithecus rosalia. Int. J. Primatol. 24(6): 1281-1300.

    Google Scholar 

  • French, J. A., de Vleeschouwer, K., Bales, K., and Heistermann, M. (2002) Lion tamarin reproductive biology. In Kleiman, D. G., and Rylands, A. B. (eds.), Lion Tamarins: Biology and Conservation, Smithsonian Institution Press, Washington, DC, pp. 133-156.

    Google Scholar 

  • French, J. A., and Inglett, B. J. (1989) Female–female aggression and male indifference in response to unfamiliar intruders in lion tamarins. Anim. Behav. 37(3): 487-497.

    Google Scholar 

  • Garber, P. A. (1997) One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy. Evol. Anthropol. 6: 187-199.

    Google Scholar 

  • Garber, P. A., and Leigh, S. R. (1997) Ontogenetic variation in small-bodied New World primates: Implications for patterns of reproduction and infant care. Folia Primatol. 68: 1-22.

    Google Scholar 

  • Garber, P. A., Moya, L., and Malaga, C. (1984) A preliminary field study of the moustached tamarin monkey (Saguinus mystax) in northeastern Peru: Questions concerned with the evolution of a communal breeding system. Folia Primatol. 42: 17-32.

    Google Scholar 

  • Garber, P. A., Pruetz, J. D., and Isaacson, J. (1993) Patterns of range use, range defense, and intergroup spacing in moustached tamarin monkeys (Saguinus mystax).Primates 34(1): 11-25.

    Google Scholar 

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

    Google Scholar 

  • Goldizen, A. W. (1988) Tamarin and marmoset mating systems: Unusual flexibility. Trends Ecol. Evol. 3: 36-40.

    Google Scholar 

  • Goldizen, A. W. (1990) A comparative perspective on the evolution of tamarin and marmoset social systems. Int. J. Primatol. 11(1): 63-83.

    Google Scholar 

  • Goldizen, A. W., Terborgh, J., Cornejo, F., Porras, D. T., and Evans, R. (1988) Seasonal food shortage, weight loss, and the timing of births in saddle-back tamarins (Saguinus fuscicollis).J. Anim. Ecol. 57: 893-901.

    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 

  • Heistermann, M., Möstl, E., and Hodges, J. K. (1995) Non-invasive endocrine monitoring of female reproductive status: methods and applications to captive breeding and conservation of exotic species. In Gansloßer, U., Hodges, J. K., and Kaumanns, W. (eds.), Research and Captive Propagation, Filander Verlag GmbH, Erlangen, pp. 36-48.

    Google Scholar 

  • Heistermann, M., Pröve, E., Wolters, H.-J., and Mika, G. (1987) Urinary oestrogen and progesterone excretion before and during pregnancy in a pied bare-face tamarin (Saguinus bicolor bicolor).J. Reprod. Fertil. 80: 635-640.

    Google Scholar 

  • Heistermann, M., Tari, S., and Hodges, J. K. (1993) Measurement of faecal steroids for monitoring ovarian function in New World primates, Callitrichidae. J. Reprod. Fertil 99: 243-251.

    Google Scholar 

  • Heymann, E. W. (1995) Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru. J. Zool., Lond. 237: 211-226.

    Google Scholar 

  • Heymann, E. W. (1996) Social behavior of wild moustached tamarins, Saguinus mystax, at the Estación Biológica Quebrada Blanco, Peruvian Amazonia. Am. J. Primatol. 38: 101-113.

    Google Scholar 

  • Heymann, E. W. (2000) The number of adult males in callitrichine groups and its implications for callitrichine social evolution. In Kappeler, P. M. (ed.), Primate Males—Causes and Consequences of Variation in Group Composition, Cambridge University Press, Cambridge, pp. 64-71.

    Google Scholar 

  • Heymann, E. W., and Buchanan-Smith, H. M. (2000) The behavioural ecology of mixed-species troops of callitrichine primates. Biol. Rev. 75: 169-190.

    Google Scholar 

  • Huck, M., Löttker, P., Böhle, U.-R., and Heymann, E. W. (submitted). All males are equal but some are more equal: Paternity and kinship patterns in polyandrous moustached tamarins(Saguinus mystax).

  • Inglett, B. J., French, J. A., Simmons, L. G., and Vires, K. W. (1989) Dynamics of intrafamily aggression and social reintegration in lion tamarins. Zoo Biol. 8: 67-78.

    Google Scholar 

  • Knogge, C., and Heymann, E. W. (2003) Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: Diversity and characteristics of plant species. Folia Primatol. 74: 33-47.

    Google Scholar 

  • Kraus, C., Heistermann, M., and Kappeler, P. M. (1999) Physiological suppression of sexual function of subordinate males: A subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiol. Behav. 66(5): 855-861.

    Google Scholar 

  • Kuederling, I., Evans, C. S., Abbott, D. H., Pryce, C. R., and Epple, G. (1995) Differential excretion of urinary oestrogen by breeding females and daughters in the red-bellied tamarin (Saguinus labiatus).Folia Primatol. 64: 140-145.

    Google Scholar 

  • Nievergelt, C. M., Digby, L. J., Ramakrishnan, U., and Woodruff, D. S. (2000) Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. Int. J. Primatol. 21(1): 1-20.

    Google Scholar 

  • Ostner, J., and Heistermann, M. (2003) Endocrine characterization of female reproductive status in wild redfronted lemurs (Eulemur fulvus rufus).Gen. Comp. Endocrinol. 131: 274-283.

    Google Scholar 

  • Peres, C. A. (1994) Primate responses to phenological changes in an Amazonian terra firme forest. Biotropica 26(1): 98-112.

    Google Scholar 

  • Ramirez, M. M. (1989) Feeding Ecology and Demography of the Moustached Tamarin Saguinus mystax in Northeastern Peru, PhD Dissertation, City University of New York, New York.

  • Saltzman, W. (2003) Reproductive competition among female common marmosets (Callithrix jacchus): Proximate and ultimate causes. In Jones, C. B. (ed.), Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions [Special Topics in Primatology, Vol. 3], American Society of Primatologists, Norman, Oklahoma, pp. 197-230.

    Google Scholar 

  • Sánchez, S., Pelaez, F., Gil-Bürmann, C., and Kaumanns, W. (1999) Costs of infant-carrying in the cotton-top tamarin (Saguinus oedipus).Am. J. Primatol. 48: 99-111.

    Google Scholar 

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

    Google Scholar 

  • Savage, A., Shideler, S. E., Soto, L. H., Causado, J., Giraldo, L. H., Lasley, B. L., and Snowdon, C. T. (1997) Reproductive events of wild cotton-top tamarins (Saguinus oedipus) in Colombia. Am. J. Primatol. 43: 329-337.

    Google Scholar 

  • Savage, A., Snowdon, C. T., Giraldo, L. H., and Soto, L. H. (1996b) Parental care patterns and vigilance in wild cotton-top tamarins (Saguinus oedipus).In Norconk, M. A., Rosenberger, A. L., and Garber, P. A. (eds.), Adaptive Radiations of Neotropical Primates, Plenum, New York, pp. 187-199.

    Google Scholar 

  • Shideler, S. E., Ortuno, A. M., Moran, F. M., Moorman, E. A., and Lasley, B. L. (1993) Simple extraction and enzyme immunoassays for estrogen and progesterone metabolites in the feces of Macaca fascicularis during non-conceptive and conceptive ovarian cycles. Biol. Reprod. 48(6): 1290-1298.

    Google Scholar 

  • Sicchar, L. A., and Heymann, E. W. (1992) Preliminary observations on external signs of estrus in moustached tamarins, Saguinus mystax (Callitrichidae). Lab. Primate Newsl. 31: 4-6.

    Google Scholar 

  • Smith, A. C., Tirado Herrera, E. R., Buchanan-Smith, H. M., and Heymann, E. W. (2001) Multiple breeding females and allo-nursing in a wild group of moustached tamarins (Saguinus mystax).Neotrop. Primates 9(2): 67-69.

    Google Scholar 

  • Snowdon, C. T., and Soini, P. (1988) The tamarins, genus Saguinus. In Mittermeier, R. A., Rylands, A. B., Coimba-Filho, A., and Fonseca, G. A. (eds.), Ecology and Behavior of neotropical primates, Vol. 2, World Wildlife Fund, Washington, DC, pp. 223-298.

  • Soini, P., and Soini, M. (1990) Distribucion geografica y ecologia poblacional de Saguinus mystax. In Castro-Rodríguez, N. E. (ed.), La Primatología en el Perú, Imprenta Propaceb, Lima, pp. 272-313.

    Google Scholar 

  • Sousa, M. B. C., and Ziegler, T. E. (1998) Diurnal variation on the excretion patterns of fecal steroids in common marmosets (Callithrix jacchus) females. Am. J. Primatol. 46: 105-117.

    Google Scholar 

  • Tardif, S. D. (1984) Social influences on sexual maturation of female Saguinus oedipus oedipus. Am. J. Primatol. 6: 199-209.

    Google Scholar 

  • Tardif, S. D., Harrison, M. L., and Simek, M. A. (1993) Communal infant care in marmosets and tamarins: Relation to energetics, ecology, and social organization. In Rylands, A. B. (ed.), Marmosets and Tamarins—Systematics, Behaviour, and Ecology, Oxford Science Publications, Oxford, pp. 220-234.

    Google Scholar 

  • Villavicencio, E., Montoya, E., and Málaga, C. (1990) Aspectos reproductivos y sanitarios de la colonia de Saguinus mystax del Centro de Reproducción y Conservación de Primates No Humanos. Iquitos, Perú. In Castro-Rodríguez, N. E. (ed.), La Primatología en el Perú, Imprenta Propaceb, Lima, pp. 589-595.

    Google Scholar 

  • Wasser, S. K., and Barash, D. P. (1983) Reproductive suppression among female mammals: Implications for biomedicine and sexual selection theory. Q. Rev. Biol. 58: 513-538.

    Google Scholar 

  • Wasser, S. K., Risler, L., and Steiner, R. A. (1988) Excreted steroids in primate feces over the menstrual cycle and pregnancy. Biol. Reprod. 39: 862-872.

    Google Scholar 

  • Wasser, S. K., Thomas, R., Nair, P. P., Guidry, C., Southers, J., Lucas, J., Wildt, D. E., and Monfort, S. L. (1993) Effects of dietary fibre on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus).J. Reprod. Fertil. 97: 569-574.

    Google Scholar 

  • Widowski, T. M., Ziegler, T. E., Elowson, A. M., and Snowdon, C. T. (1990) The role of males in the stimulation of reproductive function in female cotton-top tamarins, Saguinus o. oedipus. Anim. Behav. 40(4): 731-741.

    Google Scholar 

  • Ziegler, T., Hodges, K., Winkler, P., and Heistermann, M. (2000) Hormonal correlates of reproductive seasonality in wild female Hanuman langurs (Presbytis entellus).Am. J. Primatol. 51: 119-134.

    Google Scholar 

  • Ziegler, T. E., Bridson, W. E., Snowdon, C. T., and Eman, S. (1987) Urinary gonadotropin and estrogen excretion during the postpartum estrus, conception, and pregnancy in the cotton-top tamarin (Saguinus oedipus oedipus).Am. J. Primatol. 12: 127-140.

    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., Scheffler, G., Wittwer, D. J., Schultz-Darken, N., Snowdon, C. T., and Abbott, D. H. (1996) Metabolism of reproductive steroids during the ovarian cycle in two species of callitrichids, Saguinus oedipus and Callithrix jacchus, and estimation of the ovulatory period from fecal steroids. Biol. Reprod. 54: 91-99.

    Google Scholar 

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Authors and Affiliations

  1. Abteilung Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, 37077, Göttingen, Germany

    Petra Löttker, Maren Huck & Eckhard W. Heymann

  2. Institut für Neuro- und Verhaltensbiologie, Abteilung Verhaltensbiologie, Westfälische Wilhelms-Universität Münster, Germany

    Petra Löttker

  3. Lehrstuhl für Verhaltensforschung, Universität Bielefeld, Germany

    Maren Huck

  4. Abteilung Reproduktionsbiologie, Deutsches Primatenzentrum, Göttingen, Germany

    Michael Heistermann

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  1. Petra Löttker
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Correspondence to Petra Löttker.

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Löttker, P., Huck, M., Heymann, E.W. et al. Endocrine Correlates of Reproductive Status in Breeding and Nonbreeding Wild Female Moustached Tamarins. International Journal of Primatology 25, 919–937 (2004). https://doi.org/10.1023/B:IJOP.0000029129.52481.e4

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