Abstract
In captive callitrichid primates, female reproductive function tends to vary with social status. However, little is known about the interplay between these factors in wild groups. We report observations on normative ovarian function in dominant and subordinate female golden lion tamarins (Leontopithecus rosalia) living in wild groups. We monitored ovarian status by measuring, via enzyme immunoassay, concentrations of excreted pregnanediol glucuronide (PdG) and estrone conjugates (E1C) in fecal samples collected noninvasively from individuals in social groups in the Poço das Antas Biological Reserve, Rio de Janeiro State, Brazil. Dominant breeding females demonstrated steroid levels similar to those previously reported for wild cotton-top tamarin females, with statistically significant rises during pregnancy. The duration of elevation of fecal steroids in breeding females was ca. 4 mo, which corresponds with estimates of gestation from captive studies. Low steroid concentrations from December to June suggest a seasonally-related period of infertility in female golden lion tamarins. Dominant and subordinate females demonstrated several differences in endocrine function. In general, younger females living in intact natal family groups showed no evidence of ovarian cyclicity. We noted endocrine profiles consistent with ovulation and subsequent pregnancy for behaviorally subordinate females living in groups with unrelated males or in which a reversal in female dominance status occurred. Results suggest that in addition to changes in female reproductive endocrinology associated with puberty, the regulation of reproduction in females in wild callitrichid groups can be sensitive to status and relatedness to breeding males.
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Abbott, D. H., and George, L. M. (1991). Reproductive consequences of changing social status in female common marmosets. In Box, H. O. (Ed.)Primate Responses to Environmental Change, Chapman and Hall, London, pp. 295-310.
Baker, A. J., and Dietz, J. M. (1996). Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia). Am. J. Primatol. 38: 47-56.
Baker, A. J., Bales, K., and Dietz, J. (2002). Mating system and group dynamics in lion tamarins. In Kleiman, D. G., and Rylands, A. B. (Eds.), Lion Tamarins: Biology and Conservation, Smithsonian Press, Washington, DC, pp. 188-212.
Bales, K., French, J. A., and Dietz, J. (2002). Explaining variation in maternal care in a cooperatively breeding species. Anim. Behav. 63: 453-461.
Carlson, A. A., Ziegler, T. E., and Snowdon, C.T. (1997). Ovarian function of pygmy marmoset daughters (Cebuella pygmaea) in intact and motherless families. Am. J. Primatol. 43:347-355.
Chaoui, N. J., and Hasler-Gallusser, S. (1999). Incomplete sexual suppression in Leontopithecus chrysomelas: A behavioural and hormonal study in a semi-natural environment. Folia Primatol. 70:47-54.
Creel, S., Creel, N. M., Mills, M. G. L., and Monfort, S. L. (1997). Rank and reproduction in cooperatively breeding African wild dogs: Behavior and endocrine correlates. Behav. Ecol. 8: 298-306.
Creel, S. R., Creel, N. M., Wildt, D. E., Monfort, S. L. (1992). Behavioural and endocrine mechanisms of reproductive suppression in Serengeti dwarf mongooses. Anim. Behav. 43: 231-245.
Creel, S. R., Waser, P. M. (1991). Failures of reproductive suppression in dwarf mongooses (Helogale parvula): Accident or adaptation? Behav. Ecol. 2: 7-15.
Creel, S. R., Waser, P. M. (1997). Variation in reproductive suppression among dwarf mongooses: Interplay between mechanisms and evolution. In Solomon, N. G., and French, J. A. (Eds.), Cooperative Breeding in Mammals, Cambridge University Press, Cambridge, UK, pp. 150-170.
De Vleeschouwer, K., Van Elsacker, L., Heistermann, M., and Leus, K. (2000). An evaluation of the suitability of contraceptive methods in golden-headed lion tamarins (Leontopithecus chrysomelas), with emphasis on melengestrol acetate (MGA) implants: 2 Endocrinological and behavior effects. Anim. Welfare 9: 385-401.
Dietz, J. M., and Baker, A. J. (1993). Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia. Anim. Behav. 46: 1067-1078.
Dietz, J. M., Baker, A. J., and Miglioretti, D. (1994). Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia). Am. J. Primatol. 34: 115-132.
Digby, L. J. (1999). Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus). Folia Primatol. 70: 136-145.
Digby, L. J., and Ferrari, S. F. (1994). Multiple breeding females in free-ranging groups of Callithrix jacchus. Int. J. Primatol. 15: 389-397.
Fite, J. E., and French, J. A. (2000). Pre-and postpartum sex steroids in female marmosets (Callithrix kuhlii): Is there a link with infant survivorship and maternal behavior? Horm. Behav. 38:1-12.
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, UK, pp. 34-75.
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. 12: 469-478.
French, J. A., Brewer, K. J., Schaffner, C. M., Schalley, J., Hightower-Merritt, D., Smith, T. E., and Bell, S. M. (1996). Urinary steroid and gonadotropin excretion across the reproductive cycle in female black tufted-ear marmosets (Callithrix kuhli). Am. J. Primatol. 40: 231-246.
French, J. A., De Vleeschouwer, K., Bales, K., Heistermann, M. (2002). Reproductive biology of lion tamarins. In Kleiman, D. G., and Rylands, A. B., (Eds.), Lion Tamarins: Biology and Conservation, Smithsonian Press, Washington, DC, pp. 133-156.
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: 487-497.
French, J. A., and Inglett, B. J. (1991). Responses to novel social stimuli in tamarins: A comparative perspective. In Box, H.O. (ed.), Primate Responses to Environmental Change, Chapman and Hall, London, pp. 275-294.
French, J. A., Inglett, B. J., and Dethlefs, T. M. (1989). The reproductive status of nonbreeding groups members in captive golden lion tamarin social groups. Am. J. Primatol. 18: 73-86.
French, J. A., and Stribley, J. A. (1985). Patterns of urinary oestrogen excretion in female golden lion tamarins (Leontopithecus rosalia). J. Reprod. Fertil. 75: 537-46.
Heistermann, M., Kleiss, E., Pröve, E., Wölters, H.-J. (1989). Fertility status, dominance, and scent maring behavior of family-housed female cotton-top tamarins (Saguinus oedipus) in absence of their mothers. Am. J. Primatol. 18: 177-189.
Kapke, C. A., Arcese, P., Ziegler, T. E., and Scheffler, G. R. (1999). Estradiol and progesterone metabolite concentrations in white-tailed deer (Odocoileus virginianus) feces. J. Zoo. Wildlife Med. 30: 361-371.
Kleiman, D. G. (1978). Characteristics of the reproductive and sociosexual interactions in pairs of lion tamarins (Leontopithecus rosalia) during the reproductive cycle. In Kleiman, D.G, (ed.), The Biology and Conservation of the Callitrichidae, Smithsonian Press, Washington, DC, pp. 181-190.
Küderling, I., Evans, C., 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.
Lazaro-Perea, C. (2001). Intergroup interactions in wild common marmosets, Callithrix jacchus: Territorial defence and assessment of neighbours. Anim. Behav. 62: 11-21.
Moehlman, P., and Hofer, M. (1997). Cooperative breeding, reproductive suppression, and body size in canids. In Solomon, N. G., and French, J. A. (Eds.), Cooperative Breeding in Mammals, Cambridge University Press, Cambridge, UK, pp. 76-128.
Moorman, E. A., Mendoza, S. P., Shideler, S. E., and Lasley, B. L. (2002). Excretion and measurement of estradiol and progesterone metabolites in the feces and urine of female squirrel monkeys (Saimiri sciureus). Am. J. Primatol. 57: 79-90.
Pryce, C. R., Abbott, D. H., Hodges, J. K., and Martin, R. D. (1988). Maternal behavior is related to prepartum urinary estradiol levels in red-bellied tamarin monkeys. Physiol. Behav. 44: 717-726.
Saltzman, W., Schultz-Darken, N. J., Scheffler, G., Wegner, F. H., and Abbott, D. H. (1994). Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiol. Behav. 56: 801-810.
Saltzman, W., Severin, J. M., Schultz-Darken, N. J., Abbott, D. H. (1997a). Behavioral and social correlates of escape from suppression of ovulation in female common marmosets housed with the natal family. Am. J. Primatol. 41: 1-21.
Saltzman, W., Schultz-Darken, N. J., and Abbott, D. H. (1997b). Familial influences on ovulatory function in common marmosets (Callithrix jacchus). Am. J. Primatol. 41: 159-178.
Savage, A., Ziegler, T. E., and Snowdon, C. T. (1988). Sociosexual develoment, pair bond formation, and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus). Am. J. Primatol. 14: 345-359.
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
Sousa, M. B. C., and Ziegler, T. E. (1998). Diurnal variation on the excretion patterns of fecal steroid in common marmoset (Callithrix jacchus) females. Am. J. Primatol. 46: 105-118.
Smith, T. E., Schaffner, C. M., and French, J. A. (1997). Social and developmental influences on reproductive function in female Wied's black tufted-ear marmosets (Callithrix kuhli). Horm. Behav. 31: 159-168.
Strier, K. B., and Ziegler, T. E. (1997). Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoids. Am. J. Primatol. 42: 299-310.
van Elsacker, L., Heistermann, M., Hodges, J. K., de Laet, A., and Verhayen, R. F. (1994). Preliminary results on the evaluation of contraceptive implants in golden-headed lion tamarins, Leontopithecus chrysomelas. Neotrop. Primates 2: 30-32.
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.
Whitten, P. L., Brockman, D. K., and Stavisky, R. C. (1998). Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Am. J. Phys. Anthropol, Supp. 27: 1-23.
Widowski, T. M., Ziegler, T. E., Elowson, A. M., and Snowdon, C. T. (1990). The role of males in the stimulation of reproduction function in female cotton-top tamarins, Saguinus o. oedipus. Anim. Behav. 40: 731-741.
Ziegler, T. E., Bridson, W. E., Snowdon, C. T., and Eman, S. (1987). The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions. Biol. Reprod. 37: 618-627.
Ziegler, T. E., Scheffler, G., Wittwer, D. J., Schultz-Darken, N. J., 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.
Ziegler, T. E., and Sousa, M. B. (2002) Parent-daughter relationships and social controls on fertility in female common marmosets, Callithrix jacchus. Horm. Behav. 42: 356-367.
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French, J.A., Bales, K.L., Baker, A.J. et al. Endocrine Monitoring of Wild Dominant and Subordinate Female Leontopithecus rosalia . International Journal of Primatology 24, 1281–1300 (2003). https://doi.org/10.1023/B:IJOP.0000005993.44897.ae
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DOI: https://doi.org/10.1023/B:IJOP.0000005993.44897.ae