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Moreira, C. M., dos Santos, L. P., Sousa, M. B. C., & Izar, P. (2016). Variation of glucocorticoid metabolite levels is associated with survival demands in immature and reproductive demands in adult wild black capuchins (Sapajus nigritus). International Journal of Psychological Research, 9(2), 20–29. https://doi.org/10.21500/20112084.2303
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To give up copyright, the authors allow that, International Journal of Psychological Research, distribute the work more broadly, check for the reuse by others and take care of the necessary procedures for the registration and administration of copyright; at the same time, our editorial board represents the interests of the author and allows authors to re-use his work in various forms. In response to the above, authors transfer copyright to the journal, International Journal of Psychological Research. This transfer does not imply other rights which are not those of authorship (for example those that concern about patents). Likewise, preserves the authors rights to use the work integral or partially in lectures, books and courses, as well as make copies for educational purposes. Finally, the authors may use freely the tables and figures in its future work, wherever make explicit reference to the previous publication in International Journal of Psychological Research. The assignment of copyright includes both virtual rights and forms of the article to allow the editorial to disseminate the work in the manner which it deems appropriate.
The editorial board reserves the right of amendments deemed necessary in the application of the rules of publication.
Abstract
According to the concept of allostasis and its association with energy mobilization, glucocorticoids (GCs) should parallel cumulative energy expenditure for animal survival and reproduction. Therefore, it is expected that seasonal food shortages might lead to increased levels of GCs. We tested this hypothesis by analyzing the intra-annual variation of fecal glucocorticoid metabolites (GCM) in 14 wild black capuchin monkeys (Sapajus nigritus) living in a social group in the Brazilian Atlantic Forest. We analyzed the association between GCM and social and environmental variables for the three age/sex classes (adult males, adult females and immatures [juveniles and infants]). Decreased fruit intake during the dry season increased the GCM levels of both immatures and adult males. Although fruit shortage influenced the allostasis of adult males, the variation in their GCM levels was more impacted by the breeding season. GCM levels of adult females varied during the late stage of pregnancy. These results suggest fruit consumption as the main source of allostatic load for immature animals, while reproductive costs had greater effect on adults.
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References
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Bell, R.H.V. (1971). A grazing ecosystem in the Serengeti. Scientific American. 225, 86-93.
Behie, A.M., Pavelka, M.S.M. & Chapman, C.A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology. 72, 600-606.
Bercovitch, F.B. & Ziegler, T.E. (2002). Current topics in primate Socioendocrinology. Annual Review of Anthropology. 31, 45-67.
Cavigelli, S.A. (1999). Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Animal Behavior. 57, 935– 944.
Chapman, N. H., Bonnet, J., Grivet, L., Lynn, J., Graham, N., Smith, R., ... & King, G. J. (2012). High-resolution mapping of a fruit firmness-related quantitative trait locus in tomato reveals epistatic interactions associated with a complex combinatorial locus. Plant Physiology, 159(4), 1644-1657.
Chrousos, G.P. & Gold, P.W. (1992). The concepts of stress and stress system disorders. Journal of the American Medical Association. 267, 1244-1252.
Clymer, G.A. (2006). Foraging responses to nutritional pressures in two species of cercopithecines: Macaca mulatta and Papio ursinus. Thesis, Georgia State University.
Cunha, M.S., Vivacqua, C., Fernandes, L.C. & Sousa, M.B.C. (2007). Annual variation in plasma cortisol levels in common marmosets, Callithrix jacchus. Biological Rhythm Research. 38, 373-381.
Dias, A.C., Custodio Filho, A., Franco, G.A.D.C. & Couto, H.T.Z. (1995). Estrutura do componente arbóreos em um trecho de floresta pluvial atlântica secundária – Parque Estadual Carlos Botelho. Revista do Instituto Florestal. 7, 125-155.
Emery Thompson, M., Muller, M.N., Kahlenberg, S.M., & Wrangham, R.W. (2010). Dynamics of social and energetic stress in wild female chimpanzees. Hormones and Behavior, 58(3), 440-449.
Emery Thompson, M., & Georgiev, A.V. (2014). The high price of success: costs of mating effort in male primates. International Journal of Primatology, 35(34), 609-627.
Ganzhorn, J. U. (2002). Distribution of a folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia, 131(3), 427-435.
Garber, P. A. (1988). Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour, 105(1), 18-34.
Izar, P. (2004). Female social relationship of Cebus apella nigritus in a South eastern Atlantic forest: an analysis through ecological models of primate social evolution. Behaviour. 141, 71-99.
Izar, P., Stone, A., Carnegie, S.D. & Nakai, E.S. (2009). Sexual selection, female choice and mating systems, in: Garber, P., Estrada, A., Bicca-Marques, J.C., Heymann E., and Strier, K. B. (Eds.), South American Primates: Testing New Theories in the Study of Primate Behavior, Ecology, and Conservation, New York: Springer Press, pp. 157-189.
Izar, P., Verderane, M. P., Peternelli‐dos‐Santos, L., Mendonça‐Furtado, O., Presotto, A., Tokuda, M. & Fragaszy, D. (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology. 73, 1-17.
Kleiber, M. (1961) The Fire of Life: an introduction to animal energetics. New York: Wiley.
Kriegsfeld, L.J. & Silver, R. (2006). The regulation of neuroendocrine function: timing is everything. Hormones and Behavior. 49, 557-574.
Lahoz, M.M., Nagle, C.A. & Porta, M. (2007). Cortisol response and ovarian hormones in juvenile and cycling female Cebus monkeys: effect of stress and dexamethasone. American Journal of Primatology. 69, 551-561.
Lindsay, J.R. & Nieman, L.K. (2005). The hypothalamic-pituitary-adrenal axis in pregnancy: challenges in disease detection and treatment. Endocrine Reviews. 26, 775-799.
Lynch, J.W., Ziegler, T.E. & Strier, K.B. (2002). Individual and seasonal variation in fecal testosterone and cortisol levels of wild tufted capuchin monkeys, Cebus apella nigritus. Hormones and Behavior. 41, 275–287.
Lynch, J. W., & Rímoli, J. (2000). Demography of a group of tufted capuchin monkeys (Cebus apella nigritus) at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Neotropical Primates, 8(1), 44-49.
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840(1), 33-44.
McEwen, B.S. & Wingfield, J.C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior. 43, 2-15.
McEwen, B.S. & Wingfield, J.C. (2007). Allostasis and allostatic load, In: Fink, G. (Ed.), Encyclopedia of Stress, second edition. Academic Press, New York, pp. 135–141.
McEwen, B.S. & Wingfield, J.C. (2010). "What’s in a name? Integrating homeostasis, allostasis and stress". Hormones and Behavior. 57, 105-111.
Mendonça-Furtado, O., Edaes, M., Palme, R., Rodrigues, A., Siqueira, J., & Izar, P. (2014). Does hierarchy stability influence testosterone and cortisol levels of bearded capuchin monkeys (Sapajus libidinosus) adult males? A comparison between two wild groups. Behavioural processes, 109, 79-88.
Muller, M.N., & Wrangham, R.W. (2004). Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology, 55, 332340.
Nakai, E. S., (2007). Fissão-fusão em Cebus nigritus: flexibilidade social com estratégia de ocupação de ambientes limitantes. MSc. thesis. University of São Paulo, Brazil.
Oftedal, O. T. (1992). The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philosophical Transactions of the Royal Society Biological. 334, 161-170.
Peternelli dos Santos, L.C. (2010). Diferenças sexo/etárias do Forrageamento de Cebus nigritus em área de Mata Atlântica. MSc. thesis. University of São Paulo, Brazil.
Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D. (2012). R Development Core Team: nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-115; 2014.
Presotto, A. & Izar, P. (2010). Spatial reference of black capuchin monkeys in Brazilian Atlantic Forest: egocentric or allocentric? Animal Behavior. 80, 125-132.
Romero, L.M., Dickens, M.J. & Cyr, N.E. (2009). The reactive scope model – a new model integrating homeostasis, allostasis, and stress. Hormones and Behavior. 55, 375–389.
Sapolsky, R.M. (1983). Individual differences in cortisol secretory patterns in the wild baboon: role of negative-feedback sensitivity. Endocrinology. 113, 2263–2268.
Sapolsky, R.M. (1986). Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). American Journal of Primatology. 11, 217-227.
Sapolsky, R.M., Romero L.M. & Munck, A.U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews. 21, 55–89.
Schoof, V.A.M., Jack, K.M., & Ziegler, T.E. (2014). Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone, Dihydrotestosterone, and Glucocorticoids. International Journal of Primatology, 35(34), 643-660.
Setchell, J.M., Smith, T., Wickings, E.J. & Knapp, L.A. (2008). Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx). American Journal of Primatology. 70, 1-10.
Setchell, J.M., Smith, T.E., Wickings, E.J. & Knapp, L.A. (2010). Stress, social behaviour, and secondary sexual traits in a male primate. Hormones and Behavior 58(5), 720-728.
Sousa, M.B.C. & Ziegler, T.E. (1998). Diurnal variation on the excreted patterns of fecal steroids in common marmosets (Callithrix jacchus) females. American Journal of Primatology. 46, 105– 117.
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.
Taira, J., (2007). Consumo de palmito juçara (Euterpe edulis Mart.) por macacos-prego (Cebus nigritus): estratégia de forrageamento ótimo ou requinte de um gourmet? MSc. thesis. University of São Paulo, Brazil.
Tardif, S.D., Ziegler, T.E., Power, M. & Layne, D.G. (2005). Endocrine changes in full-term pregnancies and pregnancy loss due to energy restriction in the common marmoset (Callithrix jacchus). The Journal of clinical endocrinology and metabolism. 90, 335–339.
Torres-Farfan, C., Valenzuela, F.J., Ebensperger, R., Mendez, N., Campino, C., Richter, H.G., Valenzuela, G.J. & Seron-Ferre, M. (2008). Circadian cortisol secretion and circadian adrenal responses to ACTH are maintained in dexamethasone suppressed capuchin monkeys (Cebus apella). American Journal of Primatology. 70, 93-100.
Weingrill, T., Gray, D.A., Barrett, L. & Henzi, S.P. (2004). Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Hormones and Behavior. 45, 259–269.
Wingfield, J.C. & Ramenofsky, M. (1999). Hormones and the behavioral ecology of stress. in: Baum, P.H.M. (Ed.), Stress Physiology in Animals. CRC Press, Sheffield, pp. 1-51.
Ziegler, T.E., Scheffler, G. & Snowdon, C.T. (1995). The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Hormones and Behavior. 29, 407-424.
Ziegler, T.E., Scheffler, G., Wittwer, D.J., Schultz-Darken, N., Snowdon, C.T. & 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. Biology of Reproduction. 54, 91–99.
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour. 49, 227-265.
Altmann, S.A. (1998). Foraging for survival: yearling baboons in Africa. University of Chicago Press.
Bales, K.L., French, J.A., Hostetler, C.M. & Dietz, J.M. (2005). Social and reproductive factors affecting cortisol levels in wild female golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology. 67, 25-35.
Bell, R.H.V. (1971). A grazing ecosystem in the Serengeti. Scientific American. 225, 86-93.
Behie, A.M., Pavelka, M.S.M. & Chapman, C.A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology. 72, 600-606.
Bercovitch, F.B. & Ziegler, T.E. (2002). Current topics in primate Socioendocrinology. Annual Review of Anthropology. 31, 45-67.
Cavigelli, S.A. (1999). Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Animal Behavior. 57, 935– 944.
Chapman, N. H., Bonnet, J., Grivet, L., Lynn, J., Graham, N., Smith, R., ... & King, G. J. (2012). High-resolution mapping of a fruit firmness-related quantitative trait locus in tomato reveals epistatic interactions associated with a complex combinatorial locus. Plant Physiology, 159(4), 1644-1657.
Chrousos, G.P. & Gold, P.W. (1992). The concepts of stress and stress system disorders. Journal of the American Medical Association. 267, 1244-1252.
Clymer, G.A. (2006). Foraging responses to nutritional pressures in two species of cercopithecines: Macaca mulatta and Papio ursinus. Thesis, Georgia State University.
Cunha, M.S., Vivacqua, C., Fernandes, L.C. & Sousa, M.B.C. (2007). Annual variation in plasma cortisol levels in common marmosets, Callithrix jacchus. Biological Rhythm Research. 38, 373-381.
Dias, A.C., Custodio Filho, A., Franco, G.A.D.C. & Couto, H.T.Z. (1995). Estrutura do componente arbóreos em um trecho de floresta pluvial atlântica secundária – Parque Estadual Carlos Botelho. Revista do Instituto Florestal. 7, 125-155.
Emery Thompson, M., Muller, M.N., Kahlenberg, S.M., & Wrangham, R.W. (2010). Dynamics of social and energetic stress in wild female chimpanzees. Hormones and Behavior, 58(3), 440-449.
Emery Thompson, M., & Georgiev, A.V. (2014). The high price of success: costs of mating effort in male primates. International Journal of Primatology, 35(34), 609-627.
Ganzhorn, J. U. (2002). Distribution of a folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia, 131(3), 427-435.
Garber, P. A. (1988). Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour, 105(1), 18-34.
Izar, P. (2004). Female social relationship of Cebus apella nigritus in a South eastern Atlantic forest: an analysis through ecological models of primate social evolution. Behaviour. 141, 71-99.
Izar, P., Stone, A., Carnegie, S.D. & Nakai, E.S. (2009). Sexual selection, female choice and mating systems, in: Garber, P., Estrada, A., Bicca-Marques, J.C., Heymann E., and Strier, K. B. (Eds.), South American Primates: Testing New Theories in the Study of Primate Behavior, Ecology, and Conservation, New York: Springer Press, pp. 157-189.
Izar, P., Verderane, M. P., Peternelli‐dos‐Santos, L., Mendonça‐Furtado, O., Presotto, A., Tokuda, M. & Fragaszy, D. (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology. 73, 1-17.
Kleiber, M. (1961) The Fire of Life: an introduction to animal energetics. New York: Wiley.
Kriegsfeld, L.J. & Silver, R. (2006). The regulation of neuroendocrine function: timing is everything. Hormones and Behavior. 49, 557-574.
Lahoz, M.M., Nagle, C.A. & Porta, M. (2007). Cortisol response and ovarian hormones in juvenile and cycling female Cebus monkeys: effect of stress and dexamethasone. American Journal of Primatology. 69, 551-561.
Lindsay, J.R. & Nieman, L.K. (2005). The hypothalamic-pituitary-adrenal axis in pregnancy: challenges in disease detection and treatment. Endocrine Reviews. 26, 775-799.
Lynch, J.W., Ziegler, T.E. & Strier, K.B. (2002). Individual and seasonal variation in fecal testosterone and cortisol levels of wild tufted capuchin monkeys, Cebus apella nigritus. Hormones and Behavior. 41, 275–287.
Lynch, J. W., & Rímoli, J. (2000). Demography of a group of tufted capuchin monkeys (Cebus apella nigritus) at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Neotropical Primates, 8(1), 44-49.
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840(1), 33-44.
McEwen, B.S. & Wingfield, J.C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior. 43, 2-15.
McEwen, B.S. & Wingfield, J.C. (2007). Allostasis and allostatic load, In: Fink, G. (Ed.), Encyclopedia of Stress, second edition. Academic Press, New York, pp. 135–141.
McEwen, B.S. & Wingfield, J.C. (2010). "What’s in a name? Integrating homeostasis, allostasis and stress". Hormones and Behavior. 57, 105-111.
Mendonça-Furtado, O., Edaes, M., Palme, R., Rodrigues, A., Siqueira, J., & Izar, P. (2014). Does hierarchy stability influence testosterone and cortisol levels of bearded capuchin monkeys (Sapajus libidinosus) adult males? A comparison between two wild groups. Behavioural processes, 109, 79-88.
Muller, M.N., & Wrangham, R.W. (2004). Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology, 55, 332340.
Nakai, E. S., (2007). Fissão-fusão em Cebus nigritus: flexibilidade social com estratégia de ocupação de ambientes limitantes. MSc. thesis. University of São Paulo, Brazil.
Oftedal, O. T. (1992). The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philosophical Transactions of the Royal Society Biological. 334, 161-170.
Peternelli dos Santos, L.C. (2010). Diferenças sexo/etárias do Forrageamento de Cebus nigritus em área de Mata Atlântica. MSc. thesis. University of São Paulo, Brazil.
Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D. (2012). R Development Core Team: nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-115; 2014.
Presotto, A. & Izar, P. (2010). Spatial reference of black capuchin monkeys in Brazilian Atlantic Forest: egocentric or allocentric? Animal Behavior. 80, 125-132.
Romero, L.M., Dickens, M.J. & Cyr, N.E. (2009). The reactive scope model – a new model integrating homeostasis, allostasis, and stress. Hormones and Behavior. 55, 375–389.
Sapolsky, R.M. (1983). Individual differences in cortisol secretory patterns in the wild baboon: role of negative-feedback sensitivity. Endocrinology. 113, 2263–2268.
Sapolsky, R.M. (1986). Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). American Journal of Primatology. 11, 217-227.
Sapolsky, R.M., Romero L.M. & Munck, A.U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews. 21, 55–89.
Schoof, V.A.M., Jack, K.M., & Ziegler, T.E. (2014). Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone, Dihydrotestosterone, and Glucocorticoids. International Journal of Primatology, 35(34), 643-660.
Setchell, J.M., Smith, T., Wickings, E.J. & Knapp, L.A. (2008). Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx). American Journal of Primatology. 70, 1-10.
Setchell, J.M., Smith, T.E., Wickings, E.J. & Knapp, L.A. (2010). Stress, social behaviour, and secondary sexual traits in a male primate. Hormones and Behavior 58(5), 720-728.
Sousa, M.B.C. & Ziegler, T.E. (1998). Diurnal variation on the excreted patterns of fecal steroids in common marmosets (Callithrix jacchus) females. American Journal of Primatology. 46, 105– 117.
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.
Taira, J., (2007). Consumo de palmito juçara (Euterpe edulis Mart.) por macacos-prego (Cebus nigritus): estratégia de forrageamento ótimo ou requinte de um gourmet? MSc. thesis. University of São Paulo, Brazil.
Tardif, S.D., Ziegler, T.E., Power, M. & Layne, D.G. (2005). Endocrine changes in full-term pregnancies and pregnancy loss due to energy restriction in the common marmoset (Callithrix jacchus). The Journal of clinical endocrinology and metabolism. 90, 335–339.
Torres-Farfan, C., Valenzuela, F.J., Ebensperger, R., Mendez, N., Campino, C., Richter, H.G., Valenzuela, G.J. & Seron-Ferre, M. (2008). Circadian cortisol secretion and circadian adrenal responses to ACTH are maintained in dexamethasone suppressed capuchin monkeys (Cebus apella). American Journal of Primatology. 70, 93-100.
Weingrill, T., Gray, D.A., Barrett, L. & Henzi, S.P. (2004). Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Hormones and Behavior. 45, 259–269.
Wingfield, J.C. & Ramenofsky, M. (1999). Hormones and the behavioral ecology of stress. in: Baum, P.H.M. (Ed.), Stress Physiology in Animals. CRC Press, Sheffield, pp. 1-51.
Ziegler, T.E., Scheffler, G. & Snowdon, C.T. (1995). The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Hormones and Behavior. 29, 407-424.
Ziegler, T.E., Scheffler, G., Wittwer, D.J., Schultz-Darken, N., Snowdon, C.T. & 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. Biology of Reproduction. 54, 91–99.
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