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Sociodemographic Correlates of Fecal Androgen Levels in Wild Male White-Handed Gibbons (Hylobates lar)

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Abstract

Despite the central role of testosterone in influencing many aspects of the male life cycle, information on the influence of social and behavioral factors associated with androgen output is available for only a few primate species, mainly those living in multimale–multifemale societies. We collected 322 fecal samples and measured fecal testosterone metabolite levels in 19 adult male white-handed gibbons (Hylobates lar) from 13 groups living in the Khao Yai National Park, Thailand, to examine the extent to which androgen output is related to sociodemographic variables (social organization, social status, presence of infants, age) in a socially flexible species, i.e., pair-living/multimale groups. We predicted that androgen levels would be higher in males 1) that live in potentially more unstable single-male/single-female units; 2) that are primary (dominant) vs. secondary; 3) that live in groups with dependent infants; and 4) that are of prime vs. senior age. We found marked differences in androgen levels among males and a significant effect of time of the year. Males living in pairs exhibited significantly higher androgen concentrations vs. males living in multimale groups, and males residing in groups with infants showed a significant increase in androgen levels throughout the sampling year. However, we found no relationship with male age or social status. The increased androgen output found in both pair-living males and those residing with infants might be a physiological mechanism that facilitates male aggression to cope with potential threats posed by social challenges and the demand for infant/group defense, respectively. More generally, our data indicate that in socially flexible species male androgen output is less strongly linked to key life-history variables than in species that live permanently in multimale–multifemale groups.

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References

  • Alberts, S. C., Sapolsky, R. M., & Altmann, J. (1992). Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Hormones and Behavior, 26, 167–178.

    Article  PubMed  CAS  Google Scholar 

  • Aujard, F., & Perret, M. (1998). Age-related effects of reproductive function and sexual competition in the male prosimian primate, Microcebus murinus. Physiology and Behavior, 64, 513–519.

    Article  PubMed  CAS  Google Scholar 

  • Baayen, R. H. (2008a). Analyzing linguistic data. Cambridge, UK: Cambridge University Press.

    Book  Google Scholar 

  • Baayen, R. H. (2008b). languageR: data sets and functions with “Analyzing Linguistic Data: a practical introduction to statistics.” R-package version 0.953.

  • Barelli, C., Heistermann, M., Boesch, C., & Reichard, U. H. (2007). Sexual swellings in wild white-handed gibbon females (Hylobates lar) indicate the probability of ovulation. Hormones and Behavior, 51, 221–230.

    Article  PubMed  CAS  Google Scholar 

  • Barelli, C., Heistermann, M., Boesch, C., & Reichard, U. H. (2008). Mating patterns and sexual swellings in pair-living and multimale groups of wild white-handed gibbons (Hylobates lar). Animal Behaviour, 75, 991–1001.

    Article  Google Scholar 

  • Bates, D., & Maechler, M. (2009). lme4: Linear mixed-effects models using S4 classes. R-package version 0.99375-31.

  • Beehner, J. C., Bergman, T. J., Cheney, D. L., Seyfarth, R. L., & Whitten, P. L. (2006). Testosterone predicts future dominance rank and mating activity among male chacma baboons. Behavioral Ecology and Sociobiology, 59, 469–479.

    Article  Google Scholar 

  • Beehner, J. C., Gesquiere, L., Seyfarth, R. M., Cheney, D. L., Alberts, S. C., & Altmann, J. (2009). Testosterone related to age and life-history stages in male baboons and geladas. Hormones and Behavior, 56, 472–480.

    Article  PubMed  CAS  Google Scholar 

  • Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., & White, J.-S. S. (2008). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution, 24, 127–135.

    Article  Google Scholar 

  • Brockelman, W. Y., Reichard, U., Treesucon, U., & Raemakers, J. J. (1998). Dispersal, pair formation, and social structure in gibbons (Hylobates lar). Behavioral Ecology and Sociobiology, 42, 329–339.

    Article  Google Scholar 

  • Brockman, D. K., Whitten, P. L., Richard, A. F., & Schneider, A. (1998). Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. American Journal of Physical Anthropology, 105, 137–151.

    Article  PubMed  CAS  Google Scholar 

  • Brockman, D. K., Whitten, P. L., Richard, A. F., & Benander, B. (2001). Birth season testosterone levels in male Verreaux’s sifaka, Propithecus verreauxi: insights into socio-demographic factors mediating seasonal testicular function. Behavioral Ecology and Sociobiology, 49, 117–127.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dixson, A. F. (1998). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press.

    Google Scholar 

  • Engqvist, L. (2005). The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Animal Behaviour, 70, 967–971.

    Article  Google Scholar 

  • Folstad, I., & Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, 603–622.

    Article  Google Scholar 

  • Girard-Buttoz, C., Heistermann, M., Krummel, S., & Engelhardt, A. (2009). Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiology and Behavior, 98, 168–175.

    Article  PubMed  CAS  Google Scholar 

  • Goldizen, A. W. (2003). Social monogamy and its variations in callitrichids: Do these relate to the costs of infant care? In U. H. Reichard & C. Boesch (Eds.), Monogamy: Mating strategies and partnerships in birds, humans and other mammals (pp. 232–247). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Gray, P. B., Yang, C. J., & Pope, H. G. (2006). Fathers have lower salivary testosterone levels than unmarried men and married non-fathers in Beijing, China. Proceedings of the Royal Society of London B: Biological Sciences, 273, 333–339.

    Article  CAS  Google Scholar 

  • Heistermann, M., Finke, M., & Hodges, J. K. (1995). Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and faecal steroid excretion patterns. American Journal of Primatology, 37, 275–284.

    Article  CAS  Google Scholar 

  • Heyland, A., Hodin, J., & Reitzel, A. M. (2005). Hormone signaling in evolution and development: a non-model system approach. BioEssays, 27, 64–75.

    Article  PubMed  CAS  Google Scholar 

  • Higham, J. P., MacLarnon, A. M., Heistermann, M., Ross, C., & Semple, S. (2009). Rates of self-directed behaviour and faecal glucocorticoid levels are not correlated in female wild olive baboons (Papio hamadryas anubis). Stress, 6, 526–532.

    Article  Google Scholar 

  • Huck, M., Löttker, P., Heymann, E. W., & Heistermann, M. (2005). Characterization and social correlates of fecal testosterone and cortisol excretion in wild male Saguiuns mystax. International Journal of Primatology, 26, 159–179.

    Article  Google Scholar 

  • Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707–740.

    Article  Google Scholar 

  • Kraus, C., Heistermann, M., & Kappeler, P. M. (1999). Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiology and Behavior, 66, 855–861.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maggioncalda, A. N., Sapolsky, R. M., & Czekala, N. M. (1999). Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. American Journal of Physical Anthropology, 109, 19–32.

    Article  PubMed  CAS  Google Scholar 

  • Marler, C. A., & Moore, M. C. (1988). Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behavioral Ecology and Sociobiology, 23, 21–26.

    Article  Google Scholar 

  • McGlothlin, J. W., Jawor, J. M., & Ketterson, E. D. (2007). Natural variation in a testosterone mediated trade-off between mating effort and parental effort. American Naturalist, 170, 864–875.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Moreno, J., Sanz, J. J., & Arriero, E. (1999). Reproductive effort and T-lymphocyte cell-mediated immunoconmpetence in female pied flycatchers (Ficedula hypoleuca). Proceedings of the Royal Society of London B: Biological Sciences, 266, 1105–1109.

    Article  Google Scholar 

  • Morrow, C. J., Kolver, E. S., Verkerk, G. A., & Matthews, L. R. (2002). Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle. General and Comparative Endocrinology, 126, 229–241.

    Article  PubMed  CAS  Google Scholar 

  • Muller, M. N., & Wrangham, R. W. (2004). Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’. Animal Behaviour, 67, 113–123.

    Article  Google Scholar 

  • Muller, M. N., Marlowe, F. W., Bugumba, R., & Ellison, P. T. (2009). Testosterone and paternal care in East African foragers and pastoralists. Proceedings of the Royal Society of London B: Biological Sciences, 276, 347–354.

    Article  Google Scholar 

  • Nunes, S., Fite, J. E., & French, J. A. (2000). Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii). Animal Behaviour, 60, 857–865.

    Article  PubMed  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, 70–82.

    Article  PubMed  CAS  Google Scholar 

  • Ostner, J., Kappeler, P. M., & Heistermann, M. (2002). Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 52, 485–495.

    Article  Google Scholar 

  • Ostner, J., Kappeler, P. M., & Heistermann, M. (2008). Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 62, 627–638.

    Article  PubMed  Google Scholar 

  • Ostner, J., Heistermann, M., & Schülke, O. (2011). Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis). Hormones and Behavior, 59, 105–113.

    Article  PubMed  CAS  Google Scholar 

  • Owen-Ashley, N. T., Hasselquist, D., & Wingfield, J. C. (2004). Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. American Naturalist, 164, 490–505.

    Article  PubMed  Google Scholar 

  • Quinn, G. P., & Keough, M. J. (2002). Experimental designs and data analysis for biologists. Cambridge, UK: Cambridge University Press.

    Book  Google Scholar 

  • R Development Core Team. (2009). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Raemaekers, J. J., & Raemaekers, P. M. (1985). Field playback of loud calls to gibbons (Hylobates lar): territorial, sex-specific and species-specific responses. Animal Behaviour, 33, 481–493.

    Article  Google Scholar 

  • Reed, W. L., Clark, M. E., Parker, P. G., Raouf, S. A., Arguedas, N., Monk, D. S., Snajdr, E., Nolan, V., Jr., & Ketterson, E. D. (2006). Physiological effects on demography: a long-term experimental study of testosterone’s effects on fitness. American Naturalist, 167, 667–683.

    Article  PubMed  CAS  Google Scholar 

  • Reichard, U. H. (2009). Social organization and mating system of Khao Yai white handed gibbons, 1992–2006. In S. M. Lappan & D. Whittaker (Eds.), Wild gibbon populations: New understandings of small ape socioecology, population biology and conservation (pp. 347–384). Berlin: Springer.

    Google Scholar 

  • Reichard, H. U., & Barelli, C. (2008). Life history and reproductive strategies of Khao Yai Hylobates lar: Implications for social evolution in apes. International Journal of Primatology, 29, 823–844.

    Article  Google Scholar 

  • Reichard, U. H., Ganpanakngan, M., & Barelli, C. (2012). White-handed gibbons of Khao Yai: Social flexibility, complex, reproductive strategies, and a slow life history. In P. M. Kappeler, & D. Watts (Eds.), Long-term field studies of primates (pp. 237–258). Heidelberg: Springer.

    Chapter  Google Scholar 

  • Robbins, M., & Czekala, N. M. (1997). A preliminary analysis of urinary testosterone and cortisol levels in wild male mountain gorillas. American Journal of Primatology, 43, 51–64.

    Article  PubMed  CAS  Google Scholar 

  • Sannen, A., Heistermann, A., van Elsacker, L., Moehle, U., & Eens, M. (2003). Urinary testosterone metabolite levels in bonobos: a comparison with chimapnzees in relation to social system. Behaviour, 140, 683–696.

    Article  Google Scholar 

  • Sapolsky, R. M. (1993). The physiology of dominance in stable versus unstable social hierarchies. In W. A. Mason & S. P. Mendoza (Eds.), Primate social conflict (pp. 171–204). Albany: SUNY Press.

    Google Scholar 

  • Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2008). Social correlates of testosterone and ornamentation in male mandrills. Hormones and Behavior, 54, 365–372.

    Article  PubMed  CAS  Google Scholar 

  • Srikosamatara, S., & Hansel, T. (1996). Mammals of Khao Yai National Park. Thailand: World Wildlife Fund, Bangkok.

    Google Scholar 

  • Stoinski, T. S., Czekala, N., Lukas, K. E., & Maple, D. L. (2002). Urinary androgen and corticoid levels in captive, male western lowland gorillas (Gorilla g. gorilla): age- and social group-related differences. American Journal of Primatology, 56, 73–87.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tangtham, N. (1991). Khao Yai ecosystem: The hydrological role of Khao Yai National Park. In Proceedings of International Workshop on Conservation and Sustainable Development, 22–26 April 1991 (pp. 345–363). Thailand: AIT/Bangkok and Khao Yai National Park.

  • Weingrill, T., Willems, E. P., Zmmermann, N., Steinmetz, H., & Heistermann, M. (2011). Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.). General and Comparative Endocrinology, 172, 446–457.

  • Wiley, C. J., & Goldizen, A. W. (2003). Testosterone is correlated with courtship but not aggression in the tropical buff-banded rail, Gallirallus philippensis. Hormones and Behavior, 43, 554–560.

    Article  PubMed  CAS  Google Scholar 

  • Wingfield, J. C., Hegner, R. E., Dufty, A. M., Jr., & Balle, G. F. (1990). The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist, 136, 829–846.

    Article  Google Scholar 

  • Wingfield, J., Jacobs, J., Tramontin, A., Perfito, N., Meddle, S., Meaney, D., & Soma, K. (2000). Toward and ecological basis of hormone behavior interactions in reproduction of birds. In K. Wallen & J. Schneider (Eds.), Reproduction in context—social and environmental influences on reproduction (pp. 85–128). Cambridge, MA: The MIT Press.

    Google Scholar 

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Acknowledgments

We thank the National Research Council of Thailand (NRCT), the National Park, Wildlife and Plant Conservation Department (DNP), as well as the superintendent of Khao Yai National Park of Thailand for providing research permissions (Research Permit No. 2.3/2210) and U. H. Reichard for agreeing to conduct our project at the study site and proving data on age class. Many thanks go also to the animal keepers of the zoos at Wuppertal, Hannover, Stuttgart, and Landau for their collaboration in proving fecal samples from Hylobates lar and to M. Pirovino for providing us access to the fecal samples of H. pileatus. We thank the Thai field assistants, Tanja Wolf, Trevor Donahue, and several volunteers, who collaborated in making the data collection possible, as well as A. Heistermann and P. Kiesel for their invaluable help with the laboratory work. We also thank R. Mundry for statistical advice and J. P. Higham, J. K. Hodges, two anonymous reviewers, and the editor J. Setchell for their helpful comments on the manuscript. Financial support was provided by a postdoctoral fellowship of the Alexander von Humboldt Foundation to C. Barelli and a grant from the German Research Foundation to M. Heistermann (DFG; HE2699/6-1).

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  1. German Primate Center, Reproductive Biology Unit, 37077, Göttingen, Germany

    Claudia Barelli & Michael Heistermann

  2. Sezione di Biodiversità Tropicale, Museo delle Scienze, 38122, Trento, Italy

    Claudia Barelli

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  1. Claudia Barelli
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Barelli, C., Heistermann, M. Sociodemographic Correlates of Fecal Androgen Levels in Wild Male White-Handed Gibbons (Hylobates lar). Int J Primatol 33, 784–798 (2012). https://doi.org/10.1007/s10764-012-9606-3

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