Skip to main content
SpringerLink
Log in

Characterization and Social Correlates of Fecal Testosterone and Cortisol Excretion in Wild Male Saguinus mystax

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

Abstract

Reproductive success in male primates can be influenced by testosterone (T) and cortisol (C). We examined them in wild Saguinus mystax via fecal hormone analysis. Firstly, we wanted to characterize male hormonal status over the course of the year. Further we tested the influence of the reproductive status of the breeding female, social instability, and intergroup encounter rates on T levels, comparing the results with predictions of the challenge hypothesis (Wingfield et al., 1990). We also tested for interindividual differences in hormonal levels, possibly related to social or breeding status. We collected data during a 12-mo study on 2 groups of moustached tamarins at the Estación Biológica Quebrada Blanco in northeastern Peru. We found fairly similar T and C levels over the course of the year for all males. Yet an elevation of T shortly after the birth of infants, during the phase of ovarian inactivity of the group’s breeding female, was evident. Hormonal levels were not significantly elevated during a phase of social instability, did not correlate with intergroup encounter rates, and did not differ between breeding and nonbreeding males. Our results confirm the challenge hypothesis (Wingfield et al., 1990). The data suggest that reproductive competition in moustached tamarins is not based on endocrinological, but instead on behavioral mechanisms, possibly combined with sperm competition.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbott, D. H. (1984). Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. Am. J. Primatol. 6: 169–186.

    CAS  Google Scholar 

  • Abbott, D. H. (1993). Social conflict and reproductive suppression in marmoset and tamarin monkeys. In Mason, W. A., and Mendoza, S. P. (eds.), Primate Social Conflict, State University of New York Press, New York, pp. 331–372.

    Google Scholar 

  • Abbott, D. H., George, L. M., and Ferreira, B. R. (1992). Endocrine and behavioral constraints on reproduction in subordinate male common marmosets. Am. J. Primatol. 27: 13.

    Google Scholar 

  • Abbott, D. H., Keverne, E. B., Bercovitch, F. B., Shively, C. A., Mendoza, S. P., Saltzman, W., Snowdon, C. T., Ziegler, T. E., Banjevic, M., Garlandm, T., Jr., and Sapolsky, R. M. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 43: 67–82.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Baker, J. V., Abbott, D. H., and Saltzman, W. (1999). Social determinants of reproductive failure in male common marmosets housed with their natal family. Anim. Behav. 58(3): 501–513.

    PubMed  Google Scholar 

  • Bales, K., French, J. A., and Dietz, J. M. (2001). Reproductive and social influences on fecal cortisol levels in wild and reintroduced female golden lion tamarins. Am. J. Primatol. 51(Suppl. 1): 40–41.

    Google Scholar 

  • Barrett, G. M., Shimizu, K., Bardi, M., and Mori, A. (2002). Fecal testosterone immunoreactivity as a non-invasive index of functional testosterone dynamics in male Japanese macaques (Macaca fuscata). Primates 43(1): 29–39.

    PubMed  Google Scholar 

  • Bouissou, M.-F. (1983). Androgens, aggressive behaviour and social relationships in higher mammals. Hormone Res. 18: 43–61.

    Article  PubMed  CAS  Google Scholar 

  • Brockmann, D. K., Whitten, P. L., Richard, A. F., and Schneider, A. (1998). Reproduction in free-ranging male Propithecus verreauxi: The hormonal correlates of mating and aggression. Am. J. Phys. Anthropol. 105: 137–151.

    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. (ed.), Marmosets and Tamarins. Systematics, Behaviour, and Ecology, Oxford Science Publications, Oxford, pp. 200–219.

    Google Scholar 

  • Cavigelli, S. A. (1999). Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Anim. Behav. 57: 935–944.

    PubMed  Google Scholar 

  • Cavigelli, S. A., and Pereira, M. E. (2000). Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 37: 246–255.

    PubMed  CAS  Google Scholar 

  • Dixson, A. F. (1980). Androgens and aggressive behavior in primates: A review. Aggress. Behav. 6: 37–67.

    CAS  Google Scholar 

  • Ferreira Raminelli, J. L., Cordeiro de Sousa, M. B., Sousa Cunha, M., and Veloso Barbosa, M. F. (2001). Morning and afternoon patterns of fecal cortisol excretion among reproductive and non-reproductive male and female common marmosets. Biological Rhythm Research 32(2): 159–167.

    Google Scholar 

  • Fowler, J., and Cohen, L. (1990). Practical Statistics for Field Biology, John Wiley & Sons Ltd., Chichester.

    Google Scholar 

  • French, J. A., and Schaffner, C. M. (1995). Social and developmental influences on urinary testosterone levels in male black tufted-ear marmosets (Callithrix kuhli). Am. J. Primatol. 36(2): 123.

    Google Scholar 

  • Ginther, A. J., Carlsona, A. A., Ziegler, T. E., and Snowdon, C. T. (2002). Neonatal and Pubertal Development in Males of a Cooperatively Breeding Primate, the Cotton-Top Tamarin (Saguinus oedipus oedipus). Biol. Reprod. 66: 282–290.

    PubMed  CAS  Google Scholar 

  • Ginther, A. J., Ziegler, T. E., and Snowdon, C. T. (2001). Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment. Anim. Behav. 61(1): 65–78.

    PubMed  Google Scholar 

  • Goldizen, A. W. (1987). Tamarins and marmosets: Communal care of offspring. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies, Chicago University Press, Chicago, pp. 34–43.

    Google Scholar 

  • Harcourt, A. H. (1995). Sexual selection and sperm competition in primates: What are male genitalia good for? Evol. Anthropol. 4: 121–129.

    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.

    Article  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, Cambridge University Press, Cambridge, pp. 64–71.

    Google Scholar 

  • Heymann, E. W. (2003). Scent marking, paternal care, and sexual selection in callitrichines. In Jones, C. (ed.), Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions, American Society of Primatologists, Norman, OK, pp. 305–325.

    Google Scholar 

  • Huck, M., Löttker, P., and Heymann, E. W. (2004a). The many faces of helping: Possible costs and benefits of infant carrying and food transfer in moustached tamarins (Saguinus mystax). Behaviour 141: 915–934.

    Google Scholar 

  • Huck, M., Löttker, P., and Heymann, E. W. (2004b). Proximate mechanisms of reproductive monopolization in male moustached tamarins (Saguinus mystax). Am. J. Primatol. 64: 39–56.

    Google Scholar 

  • Huck, M., Löttker, P., Böhle, U.-R., and Heymann, E. W. (2005). Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax). Am. J. Phys. Anthropol. (in press).

  • Kholkute, S. D. (1984). Diurnal and annual variations in plasma androgen levels in the adult male marmoset (Callithrix jacchus). Physiol. Behav. 7: 431–438.

    CAS  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.

    PubMed  CAS  Google Scholar 

  • Löttker, P., Huck, M., Heymann, E. W., and Heistermann, M. (2004a). Endocrine correlates of reproductive status in breeding and non-breeding wild female moustached tamarins (Saguinus mystax). Int. J. Primatol. 25(4): 919–937.

    Google Scholar 

  • Löttker, P., Huck, M., and Heymann, E. W. (2004b). Demographic parameters and events in wild moustached tamarins (Saguinus mystax). Am. J. Primatol. 64: 425–449.

    Google Scholar 

  • Lynch, J. W., Ziegler, T. E., and Strier, K. B. (2002). Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm. Behav. 41: 275–287.

    PubMed  CAS  Google Scholar 

  • Möhle, U., Heistermann, M., Palme, R., and Hodges, J. K. (2002). Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Endocrinology 129: 135–145.

    Article  Google Scholar 

  • Moreno, J., Veiga, J. P., Cordero, P. J., and Mínguez, E. (1999). Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor. Behav. Ecol. Sociobiol. 47: 47–53.

    Google Scholar 

  • Nunes, S., Fites, J., and French, J. (2000). Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii). Anim. Behav. 60(6): 857–865.

    PubMed  Google Scholar 

  • Ostner, J., Kappeler, P. M., and Heistermann, M. (2002). Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 52: 485–495.

    Google Scholar 

  • Palme, R., and Möstl, E. (1997). Measurements of cortisol metabolites in faeces of sheep as aparameter of cortisol concentration in blood. Int. J. Mammal. Biol. 62(Suppl. II): 192–197.

    Google Scholar 

  • Sapolsky, R. M. (1982). The endocrine stress-response and social status in the wild baboon. Horm. Behav. 16: 279–292.

    PubMed  CAS  Google Scholar 

  • Sapolsky, R. M. (1985). Stress-induced suppression of testicular function in the wild baboon: Role of glucocorticoids. Endocrinology 116(6): 2273–2278.

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky, R. M. (2002). Endocrinology of the stress-response. In Becker, J. B., Breedlove, S. M., Crews, D., and McCarthy, M. M. (eds.), Behavioral Endocrinology, The MIT Press, Cambridge (Massachusetts), pp. 409–450.

    Google Scholar 

  • Snowdon, C. T., and Soini, P. (1988). The Tamarins, Genus Saguinus. In Mittermeier, R. A., Rylands, A. B., Coimbra-Filho, A., and Fonseca, G. A. B. (eds.), Ecology and Behavior of Neotropical Primates, World Wildlife Fund, Washington, pp. 223–298.

    Google Scholar 

  • Soini, P., and Soini, M. (1990). Distribución geográfica y ecológia poblacional de Saguinus mystax. In Castro-Rodríguez, N. E. (ed.), La primatología en el Perú. Investigaciones primatológicas (1973–1985), 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 marmoset (Callithrix jacchus) females. Am. J. Primatol. 46: 105–117.

    PubMed  CAS  Google Scholar 

  • Strier, K. B., Ziegler, T. E., and Wittwer, D. J. (1999). Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm. Behav. 35: 125–134.

    PubMed  CAS  Google Scholar 

  • Sussman, R. W., and Garber, P. A. (1987). A new interpretation of the social organization and mating system of the callitrichidae. Int. J. Primatol. 8(1): 73–92.

    Google Scholar 

  • Suttie, J. M., Lincoln, G. A., and Kay, R. N. B. (1984). Endocrine control of antler growth in red deer stags. J. Reprod. Fert. 71: 7–15.

    Article  CAS  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 

  • Trainor, B. C., and Marler, C. A. (2001). Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Horm. Behav. 40: 32–42.

    PubMed  CAS  Google Scholar 

  • von Engelhardt, N., Kappeler, P. M., and Heistermann, M. (2000). Androgen levels and female social dominance in Lemur catta. Proc. R. Soc. Lond. B 267: 1533–1539.

    CAS  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.

    PubMed  CAS  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. Fert. 97: 569–574.

    Article  CAS  Google Scholar 

  • Whitten, P. L., Staviesky, R., Aureli, F., and Russell, E. (1998). Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am. J. Primatol. 44: 57–69.

    PubMed  CAS  Google Scholar 

  • Wickings, E. J., Marshall, G. R., and Nieschlag, E. (1986). Endocrine regulation of male reproduction. In Dukelow, W. R., and Erwin, J. (eds.), Comparative Primate Biology, Alan R. Liss, Inc., New York, pp. 149–170.

    Google Scholar 

  • Wingfield, J. C., Hegner, R. E., Dufty, A. M. J., and Ball, G. F. (1990). The “challenge hypothesis”: Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136(6): 829–846.

    Google Scholar 

  • Ziegler, T. E., Snowdon, C. T., Schultz-Darken, N. J., and Ferris, C. F. (2003). Chemical cues of ovulation mediate androgen production in marmosets (Callithrix jacchus) and tamarins (Saguinus oedipus). Am. J. Primatol. 60(Suppl. 1): 133.

    Google Scholar 

  • Ziegler, T. E., and Sousa, M. B. C. (2002). Parent-daughter relationships and social controls on fertility in female common marmosets, Callithrix jacchus. Horm. Behav. 42: 356–367.

    PubMed  CAS  Google Scholar 

  • Ziegler, T. E., Wegner, F. H., Carlson, A. A., Lazaro-Perea, C., and Snowdon, C. T. (2000). Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): Interactions with gender, androgen levels, and parenting. Horm. Behav. 38: 111–122.

    PubMed  CAS  Google Scholar 

  • Ziegler, T. E., Wegner, F. H., and Snowdon, C. T. (1996). Hormonal responses to parental and nonparental conditions in male cotton-top tamarins, Saguinus oedipus, a new world primate. Horm. Behav. 30: 287–297.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Abteilung Soziobiologie, Deutsches Primatenzentrum, Göttingen, Germany

    Maren Huck, Petra Löttker & Eckhard W. Heymann

  2. Lehrstuhl für Verhaltensforschung, Universität Bielefeld, Germany

    Maren Huck

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

    Petra Löttker

  4. Abteilung Reproduktionsbiologie, Deutsches Primatenzentrum, Göttingen, Germany

    Michael Heistermann

  5. Abeteilung Soziobiology, Deutsches Primatenzentrum, Kellnerweg 4, D-37077, Göttingen, Germany

    Maren Huck

Authors
  1. Maren Huck
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petra Löttker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eckhard W. Heymann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Heistermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maren Huck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huck, M., Löttker, P., Heymann, E.W. et al. Characterization and Social Correlates of Fecal Testosterone and Cortisol Excretion in Wild Male Saguinus mystax . Int J Primatol 26, 159–179 (2005). https://doi.org/10.1007/s10764-005-0728-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-005-0728-8

Key words

Search

Navigation