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Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone, Dihydrotestosterone, and Glucocorticoids

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Abstract

Reproductive success is linked to dominance in male primates, reflecting the benefits of male competition. However, not all males compete successfully, suggesting that the costs of obtaining and maintaining high dominance status are significant. Here we examine the fecal metabolites of testosterone (fT) and dihydrotestosterone (fDHT) as bioactive androgens reflecting male reproductive effort, as well as fecal glucocorticoid (fGC) excretion as an index of stress in male white-faced capuchins (Cebus capucinus). We investigated the influence of female fertility (periovulatory vs. nonovulatory) on the hormonal responses of alpha and subordinate males. Over a 17-mo field season, we collected and analyzed weekly fecal samples (N = 992) from all 14 adult (> 10 yr) and subadult (≥ 6–10 yr) males residing in three study groups in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. Fecal samples (N > 2250) were also collected from group females (N = 28) to identify the fertile period using progesterone and estradiol assays. Alpha males had significantly higher fT, fDHT, and fGC levels than subordinate males independent of female reproductive state; further, adult subordinates had significantly higher fT, but not fDHT or fGC, than subadult subordinates. Male fT, fDHT, and fGC levels were significantly higher in the presence of fertile females, regardless of male dominance status and age. These findings indicate that the higher reproductive effort of alpha males comes with some costs (increased fGCs), and the presence of periovulatory females is associated with specific endocrine responses reflecting male reproductive effort and stress in white-faced capuchins.

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Acknowledgments

This study was supported by funds from the Fonds Québecois de la Recherche sur la Nature et les Technologies (V. A. M. Schoof), LSB Leakey Foundation (V. A. M. Schoof), National Geographic Society (V. A. M. Schoof, grant 8652–09), National Science Foundation (V. A. M. Schoof, grant 0926039), Tulane University’s Stone Center for Latin American Studies (V. A. M. Schoof; K. M. Jack) and Research Enhancement Fund (K. M. Jack), and a grant to the WNPRC from the National Institutes of Health (T. E. Ziegler, grant RR000167). We thank the many field assistants who were involved in data collection: T. Busch, J. Rinderknecht, S. Fatkin, D. Broome, A-S. Pellier, A. Tecza, S. Millus, L. Wilkins, R. Jackson, K. Catanese, and A. Olvarez, and J. Addicott, who provided data management consulting. We are grateful to Dan Wittwer from the WNPRC for hormone assay validations and for guidance and assistance in conducting hormone analyses. We also acknowledge the administrators of the Área de Conservación Guanacaste (especially Roger Blanco Segura) for allowing us to conduct research in the park through the present day. Finally, we thank Alexander Georgiev and Melissa Emery Thompson for inviting us to participate in this special issue, and two anonymous reviewers and the editor-in-chief for their constructive criticisms.

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Schoof, V.A.M., Jack, K.M. & Ziegler, T.E. Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone, Dihydrotestosterone, and Glucocorticoids. Int J Primatol 35, 643–660 (2014). https://doi.org/10.1007/s10764-013-9742-4

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