Skip to main content
Top
Published in: BioPsychoSocial Medicine 1/2010

Open Access 01-12-2010 | Research

The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees

Authors: Michael P Muehlenbein, David P Watts

Published in: BioPsychoSocial Medicine | Issue 1/2010

Login to get access

Abstract

Background

Male members of primate species that form multi-male groups typically invest considerable effort into attaining and maintaining high dominance rank. Aggressive behaviors are frequently employed to acquire and maintain dominance status, and testosterone has been considered the quintessential physiological moderator of such behaviors. Testosterone can alter both neurological and musculoskeletal functions that may potentiate pre-existing patterns of aggression. However, elevated testosterone levels impose several costs, including increased metabolic rates and immunosuppression. Cortisol also limits immune and reproductive functions.

Methods

To improve understanding of the relationships between dominance rank, hormones and infection status in nonhuman primates, we collected and analyzed 67 fecal samples from 22 wild adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Samples were analyzed for cortisol and testosterone levels as well as intestinal parasite prevalence and richness. 1,700 hours of observation data were used to determine dominance rank of each animal. We hypothesized that dominance rank would be directly associated with fecal testosterone and cortisol levels and intestinal parasite burden.

Results

Fecal testosterone (but not cortisol) levels were directly associated with dominance rank, and both testosterone and cortisol were directly associated with intestinal parasite richness (number of unique species recovered). Dominance rank was directly associated with helminth (but not protozoan) parasite richness, so that high ranking animals had higher testosterone levels and greater helminth burden.

Conclusions

One preliminary interpretation is that the antagonist pleiotropic effects of androgens and glucocorticoids place a cost on attaining and maintaining high dominance rank in this species. Because of the costs associated with elevated steroid levels, dominance status may be an honest signal of survivorship against helminth parasites.
Appendix
Available only for authorised users
Literature
1.
go back to reference de Ruiter J, van Hooff JARAM, Schefrahn W: Social and genetic aspects of paternity in wild long-tailed macaques. Behaviour. 1994, 129: 203-224. 10.1163/156853994X00613.CrossRef de Ruiter J, van Hooff JARAM, Schefrahn W: Social and genetic aspects of paternity in wild long-tailed macaques. Behaviour. 1994, 129: 203-224. 10.1163/156853994X00613.CrossRef
2.
go back to reference Ellis L: Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol. 1995, 16: 257-333. 10.1016/0162-3095(95)00050-U.CrossRef Ellis L: Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol. 1995, 16: 257-333. 10.1016/0162-3095(95)00050-U.CrossRef
3.
go back to reference Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacy RC, Bruford MW: Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA. 1996, 102: 338-345.CrossRef Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacy RC, Bruford MW: Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA. 1996, 102: 338-345.CrossRef
4.
go back to reference Setchell JM, Charpentier M, Wickings EJ: Mate guarding and paternity in mandrills (Mandrillus sphinx): factors influencing alpha male monopoly. Anim Behav. 2005, 70: 1105-1120. 10.1016/j.anbehav.2005.02.021.CrossRef Setchell JM, Charpentier M, Wickings EJ: Mate guarding and paternity in mandrills (Mandrillus sphinx): factors influencing alpha male monopoly. Anim Behav. 2005, 70: 1105-1120. 10.1016/j.anbehav.2005.02.021.CrossRef
5.
go back to reference Alberts SC, Buchan JC, Altmann J: Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav. 2006, 72: 1177-1196. 10.1016/j.anbehav.2006.05.001.CrossRef Alberts SC, Buchan JC, Altmann J: Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav. 2006, 72: 1177-1196. 10.1016/j.anbehav.2006.05.001.CrossRef
6.
go back to reference Englehardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C: Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis) - male monopolization, female mate choice or post-copulatory mechanisms?. Behav Ecol Sociobiol. 2006, 59: 740-752. 10.1007/s00265-005-0104-x.CrossRef Englehardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C: Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis) - male monopolization, female mate choice or post-copulatory mechanisms?. Behav Ecol Sociobiol. 2006, 59: 740-752. 10.1007/s00265-005-0104-x.CrossRef
7.
go back to reference Goodall J: The Chimpanzees of Gombe. 1986, Cambridge: Harvard University Press Goodall J: The Chimpanzees of Gombe. 1986, Cambridge: Harvard University Press
8.
go back to reference Constable J, Ashley M, Goodall J, Pusey A: Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol. 2001, 10: 1279-1300. 10.1046/j.1365-294X.2001.01262.x.PubMedCrossRef Constable J, Ashley M, Goodall J, Pusey A: Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol. 2001, 10: 1279-1300. 10.1046/j.1365-294X.2001.01262.x.PubMedCrossRef
9.
go back to reference Boesch C, Kohou G, Nene H, Vigilant L: Male competition and paternity in wild chimpanzees of the Tai Forest. Am J Phys Anthropol. 2006, 130: 103-115. 10.1002/ajpa.20341.PubMedCrossRef Boesch C, Kohou G, Nene H, Vigilant L: Male competition and paternity in wild chimpanzees of the Tai Forest. Am J Phys Anthropol. 2006, 130: 103-115. 10.1002/ajpa.20341.PubMedCrossRef
10.
go back to reference Marin P, Holmang S, Jonsson L, Sjostrom L, Kvist H, Holm G, Lindstedt G, Bjorntorp P: The effects of testosterone treatment on body composition and metabolism in middle-aged obese men. Int J Obes Relat Metab Disord. 1992, 16: 991-997.PubMed Marin P, Holmang S, Jonsson L, Sjostrom L, Kvist H, Holm G, Lindstedt G, Bjorntorp P: The effects of testosterone treatment on body composition and metabolism in middle-aged obese men. Int J Obes Relat Metab Disord. 1992, 16: 991-997.PubMed
11.
go back to reference Welle S, Jozefowicz R, Forbes G, Griggs RC: Effect of testosterone on metabolic rate and body composition in normal men and men with muscular dystrophy. J Clin Endocrinol Metab. 1992, 74: 332-335. 10.1210/jc.74.2.332.PubMed Welle S, Jozefowicz R, Forbes G, Griggs RC: Effect of testosterone on metabolic rate and body composition in normal men and men with muscular dystrophy. J Clin Endocrinol Metab. 1992, 74: 332-335. 10.1210/jc.74.2.332.PubMed
12.
go back to reference Bhasin S, Storer TW, Berman N, Callegari C, Clevenger B, Phillips J, Bunnell TJ, Tricker R, Shirazi A, Casaburi R: The effects of supraphysiological doses of testosterone on muscle size and strength in normal men. N Engl J Med. 1996, 335: 1-7. 10.1056/NEJM199607043350101.PubMedCrossRef Bhasin S, Storer TW, Berman N, Callegari C, Clevenger B, Phillips J, Bunnell TJ, Tricker R, Shirazi A, Casaburi R: The effects of supraphysiological doses of testosterone on muscle size and strength in normal men. N Engl J Med. 1996, 335: 1-7. 10.1056/NEJM199607043350101.PubMedCrossRef
13.
go back to reference Tsai LW, Sapolsky RM: Rapid stimulatory effects of testosterone upon myotubule metabolism and sugar transport, as assessed by silicon microphysiometry. Aggressive Behav. 1996, 22: 357-364. 10.1002/(SICI)1098-2337(1996)22:5<357::AID-AB4>3.0.CO;2-G.CrossRef Tsai LW, Sapolsky RM: Rapid stimulatory effects of testosterone upon myotubule metabolism and sugar transport, as assessed by silicon microphysiometry. Aggressive Behav. 1996, 22: 357-364. 10.1002/(SICI)1098-2337(1996)22:5<357::AID-AB4>3.0.CO;2-G.CrossRef
14.
go back to reference Kendrick K, Drewett R: Testosterone reduces refractory period of stria terminalis neurons in the rat brain. Science. 1979, 204: 877-10.1126/science.220709.PubMedCrossRef Kendrick K, Drewett R: Testosterone reduces refractory period of stria terminalis neurons in the rat brain. Science. 1979, 204: 877-10.1126/science.220709.PubMedCrossRef
15.
go back to reference Goy RW, McEwen BS: Sexual Differentiation of the Brain. 1979, Cambridge: MIT Press Goy RW, McEwen BS: Sexual Differentiation of the Brain. 1979, Cambridge: MIT Press
16.
go back to reference Pelliniemi LJ, Fröjdman K, Paranko J: Embryological and prenatal development and function of Sertoli cells. The Sertoli Cell. Edited by: Russell LD, Griswold MD. 1993, Clearwater, FL: Cache River Press, 87-113. Pelliniemi LJ, Fröjdman K, Paranko J: Embryological and prenatal development and function of Sertoli cells. The Sertoli Cell. Edited by: Russell LD, Griswold MD. 1993, Clearwater, FL: Cache River Press, 87-113.
17.
go back to reference Coe CL, Smith ER, Mendoza SP, Levine S: Varying influence of social status on hormone levels in male squirrel monkeys. Hormones, Drugs, and Social Behavior in Primates. Edited by: Steklis HD, Kling AS. 1983, New York: SP Medical and Scientific Books, 7-21. Coe CL, Smith ER, Mendoza SP, Levine S: Varying influence of social status on hormone levels in male squirrel monkeys. Hormones, Drugs, and Social Behavior in Primates. Edited by: Steklis HD, Kling AS. 1983, New York: SP Medical and Scientific Books, 7-21.
18.
go back to reference Bercovitch FB: Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). J Reprod Fertil. 1993, 99: 113-120. 10.1530/jrf.0.0990113.PubMedCrossRef Bercovitch FB: Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). J Reprod Fertil. 1993, 99: 113-120. 10.1530/jrf.0.0990113.PubMedCrossRef
19.
go back to reference Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A: Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav. 2002, 42: 85-96. 10.1006/hbeh.2002.1804.PubMedCrossRef Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A: Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav. 2002, 42: 85-96. 10.1006/hbeh.2002.1804.PubMedCrossRef
20.
go back to reference Lynch JW, Ziegler TE, Strier KB: Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus paella nigritus. Horm Behav. 2002, 41: 275-287. 10.1006/hbeh.2002.1772.PubMedCrossRef Lynch JW, Ziegler TE, Strier KB: Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus paella nigritus. Horm Behav. 2002, 41: 275-287. 10.1006/hbeh.2002.1772.PubMedCrossRef
21.
go back to reference Mazur A, Booth A: Testosterone and dominance in men. Behav Brain Sci. 1998, 21: 353-371. 10.1017/S0140525X98001228.PubMedCrossRef Mazur A, Booth A: Testosterone and dominance in men. Behav Brain Sci. 1998, 21: 353-371. 10.1017/S0140525X98001228.PubMedCrossRef
22.
go back to reference Archer J: Testosterone and human aggression: an evaluation of the challenge hypothesis. Neuro Biobehav Rev. 2006, 39: 319-345. 10.1016/j.neubiorev.2004.12.007.CrossRef Archer J: Testosterone and human aggression: an evaluation of the challenge hypothesis. Neuro Biobehav Rev. 2006, 39: 319-345. 10.1016/j.neubiorev.2004.12.007.CrossRef
23.
go back to reference Dixson AF, Herbert J: Testosterone, aggressive behavior and dominance rank in captive adult male talapoin monkeys (Miopithecus talapoin). Physiol Behav. 1977, 18: 534-539. 10.1016/0031-9384(77)90272-4.CrossRef Dixson AF, Herbert J: Testosterone, aggressive behavior and dominance rank in captive adult male talapoin monkeys (Miopithecus talapoin). Physiol Behav. 1977, 18: 534-539. 10.1016/0031-9384(77)90272-4.CrossRef
24.
go back to reference Wingfield JC, Hegner RE, Ball GF, Duffy AM: The 'challenge hypothesis': theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat. 1990, 136: 829-846. 10.1086/285134.CrossRef Wingfield JC, Hegner RE, Ball GF, Duffy AM: The 'challenge hypothesis': theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat. 1990, 136: 829-846. 10.1086/285134.CrossRef
25.
go back to reference Marler CA, Moore MC: Evolutionary costs of aggression revealed by testosterone manipulations in free-living lizards. Behav Ecol Sociobiol. 1988, 23: 21-26. 10.1007/BF00303053.CrossRef Marler CA, Moore MC: Evolutionary costs of aggression revealed by testosterone manipulations in free-living lizards. Behav Ecol Sociobiol. 1988, 23: 21-26. 10.1007/BF00303053.CrossRef
26.
go back to reference Ketterson ED, Nolan V: Hormones and life histories: an integrative approach. Am Nat. 1992, 140: S33-S62. 10.1086/285396.PubMedCrossRef Ketterson ED, Nolan V: Hormones and life histories: an integrative approach. Am Nat. 1992, 140: S33-S62. 10.1086/285396.PubMedCrossRef
27.
go back to reference Soronen P, Laiti M, Torn S, Harkönen P, Patrikainen L, Li Y, Pulkka A, Kurkela R, Herrala A, Kaija H, Isomaa V, Vihko P: Sex steroid hormone metabolism and prostate cancer. J Steroid Biochem Mol Biol. 2004, 92: 281-286. 10.1016/j.jsbmb.2004.10.004.PubMedCrossRef Soronen P, Laiti M, Torn S, Harkönen P, Patrikainen L, Li Y, Pulkka A, Kurkela R, Herrala A, Kaija H, Isomaa V, Vihko P: Sex steroid hormone metabolism and prostate cancer. J Steroid Biochem Mol Biol. 2004, 92: 281-286. 10.1016/j.jsbmb.2004.10.004.PubMedCrossRef
28.
go back to reference Zirkin BR, Chen H: Regulation of Leydig cell steroidogenic function during aging. Biol Reprod. 2000, 63: 977-981. 10.1095/biolreprod63.4.977.PubMedCrossRef Zirkin BR, Chen H: Regulation of Leydig cell steroidogenic function during aging. Biol Reprod. 2000, 63: 977-981. 10.1095/biolreprod63.4.977.PubMedCrossRef
29.
go back to reference Muehlenbein MP, Bribiescas RG: Testosterone-mediated immune functions and male life histories. Am J Hum Biol. 2005, 17: 527-558. 10.1002/ajhb.20419.PubMedCrossRef Muehlenbein MP, Bribiescas RG: Testosterone-mediated immune functions and male life histories. Am J Hum Biol. 2005, 17: 527-558. 10.1002/ajhb.20419.PubMedCrossRef
30.
go back to reference Stearns S: Trade-offs in life-history evolution. Funct Ecol. 1989, 3: 259-268. 10.2307/2389364.CrossRef Stearns S: Trade-offs in life-history evolution. Funct Ecol. 1989, 3: 259-268. 10.2307/2389364.CrossRef
31.
go back to reference Bribiescas RG: Reproductive ecology and life history of the human male. Yearb Phys Anthropol. 2001, 44: 148-176. 10.1002/ajpa.10025.CrossRef Bribiescas RG: Reproductive ecology and life history of the human male. Yearb Phys Anthropol. 2001, 44: 148-176. 10.1002/ajpa.10025.CrossRef
32.
go back to reference Hau M: Regulation of male life history traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays. 2007, 29: 133-144. 10.1002/bies.20524.PubMedCrossRef Hau M: Regulation of male life history traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays. 2007, 29: 133-144. 10.1002/bies.20524.PubMedCrossRef
33.
go back to reference Folstad I, Karter AJ: Parasites, bright males and the immunocompetence handicap. Am Nat. 1992, 139: 603-622. 10.1086/285346.CrossRef Folstad I, Karter AJ: Parasites, bright males and the immunocompetence handicap. Am Nat. 1992, 139: 603-622. 10.1086/285346.CrossRef
34.
go back to reference Wedekind C, Folstad I: Adaptive or nonadaptive immunosuppression by sex-hormones. Am Nat. 1994, 143: 936-938. 10.1086/285641.CrossRef Wedekind C, Folstad I: Adaptive or nonadaptive immunosuppression by sex-hormones. Am Nat. 1994, 143: 936-938. 10.1086/285641.CrossRef
35.
go back to reference Hamilton WD, Zuk M: Heritable true fitness and bright birds: a role for parasites?. Science. 1982, 218: 384-387. 10.1126/science.7123238.PubMedCrossRef Hamilton WD, Zuk M: Heritable true fitness and bright birds: a role for parasites?. Science. 1982, 218: 384-387. 10.1126/science.7123238.PubMedCrossRef
36.
go back to reference Moller AP, Petrie M: Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol. 2002, 13: 248-253. 10.1093/beheco/13.2.248.CrossRef Moller AP, Petrie M: Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol. 2002, 13: 248-253. 10.1093/beheco/13.2.248.CrossRef
37.
go back to reference Saino N, Incagli M, Martinelli R, Moller AP: Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behav Ecol. 2002, 13: 169-174. 10.1093/beheco/13.2.169.CrossRef Saino N, Incagli M, Martinelli R, Moller AP: Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behav Ecol. 2002, 13: 169-174. 10.1093/beheco/13.2.169.CrossRef
38.
go back to reference Moller AP, Kimball RT, Erritzoe J: Sexual ornamentation, condition, and immune defense in the house sparrow Passer domesticus. Behav Ecol Sociobiol. 1996, 39: 317-322. 10.1007/s002650050295.CrossRef Moller AP, Kimball RT, Erritzoe J: Sexual ornamentation, condition, and immune defense in the house sparrow Passer domesticus. Behav Ecol Sociobiol. 1996, 39: 317-322. 10.1007/s002650050295.CrossRef
39.
go back to reference Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, Van Den Bussche RA: Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution Int J Org Evolution. 2001, 55: 616-625.CrossRef Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, Van Den Bussche RA: Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution Int J Org Evolution. 2001, 55: 616-625.CrossRef
40.
go back to reference Garamszegi LZ, Moller AP, Erritzoe J: The evolution of immune defense and song complexity in birds. Evolution Int J Org Evolution. 2003, 57: 905-912.CrossRef Garamszegi LZ, Moller AP, Erritzoe J: The evolution of immune defense and song complexity in birds. Evolution Int J Org Evolution. 2003, 57: 905-912.CrossRef
41.
go back to reference Doucet SM, Montgomerie R: Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav Ecol. 2003, 14: 503-509. 10.1093/beheco/arg035.CrossRef Doucet SM, Montgomerie R: Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav Ecol. 2003, 14: 503-509. 10.1093/beheco/arg035.CrossRef
42.
go back to reference Lagesen K, Folstad I: Antler asymmetry and immunity in reindeer. Behav Ecol Sociobiol. 1998, 44: 135-142. 10.1007/s002650050524.CrossRef Lagesen K, Folstad I: Antler asymmetry and immunity in reindeer. Behav Ecol Sociobiol. 1998, 44: 135-142. 10.1007/s002650050524.CrossRef
43.
go back to reference Bradley BJ, Mundy NI: The primate palette: the evolution of primate coloration. Evol Anth. 2008, 17: 97-111. 10.1002/evan.20164.CrossRef Bradley BJ, Mundy NI: The primate palette: the evolution of primate coloration. Evol Anth. 2008, 17: 97-111. 10.1002/evan.20164.CrossRef
44.
go back to reference Folstad I, Skarstein F: Is male germ line control creating avenues for female choice?. Behav Ecol. 1997, 8: 109-112. 10.1093/beheco/8.1.109.CrossRef Folstad I, Skarstein F: Is male germ line control creating avenues for female choice?. Behav Ecol. 1997, 8: 109-112. 10.1093/beheco/8.1.109.CrossRef
45.
go back to reference Kacelnik A, Norris S: Signaling via testosterone: communicating health and vigour. Behav Brain Sci. 1998, 21: 378-385. 10.1017/S0140525X98411221.CrossRef Kacelnik A, Norris S: Signaling via testosterone: communicating health and vigour. Behav Brain Sci. 1998, 21: 378-385. 10.1017/S0140525X98411221.CrossRef
46.
go back to reference Buchanan KL: Stress and the evolution of condition-dependent signals. Trends Ecol Evol. 2000, 15: 156-160. 10.1016/S0169-5347(99)01812-1.PubMedCrossRef Buchanan KL: Stress and the evolution of condition-dependent signals. Trends Ecol Evol. 2000, 15: 156-160. 10.1016/S0169-5347(99)01812-1.PubMedCrossRef
47.
go back to reference Evans MR, Goldsmith AR, Norris SRA: The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol. 2000, 47: 156-163. 10.1007/s002650050006.CrossRef Evans MR, Goldsmith AR, Norris SRA: The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol. 2000, 47: 156-163. 10.1007/s002650050006.CrossRef
48.
go back to reference McEwen BS: Stress, adaptation, and disease: allostasis and allostatic load. Ann NY Acad Sci. 1998, 840: 33-44. 10.1111/j.1749-6632.1998.tb09546.x.PubMedCrossRef McEwen BS: Stress, adaptation, and disease: allostasis and allostatic load. Ann NY Acad Sci. 1998, 840: 33-44. 10.1111/j.1749-6632.1998.tb09546.x.PubMedCrossRef
49.
go back to reference Elenkov IJ, Papanicolaou DA, Wilder RL, Chrousos GP: Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications. Proc Assoc Am Physicians. 1996, 108: 374-381.PubMed Elenkov IJ, Papanicolaou DA, Wilder RL, Chrousos GP: Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications. Proc Assoc Am Physicians. 1996, 108: 374-381.PubMed
50.
go back to reference Norbiato G, Bevilacqua M, Vago T, Taddei A, Clerici M: Glucocorticoids and the immune function in the human immunodeficiency virus infection: a study in hypercortisolemic and cortisol-resistant patients. J Clin Endocrinol Metab. 1997, 82: 3260-3263. 10.1210/jc.82.10.3260.PubMed Norbiato G, Bevilacqua M, Vago T, Taddei A, Clerici M: Glucocorticoids and the immune function in the human immunodeficiency virus infection: a study in hypercortisolemic and cortisol-resistant patients. J Clin Endocrinol Metab. 1997, 82: 3260-3263. 10.1210/jc.82.10.3260.PubMed
51.
go back to reference Turnbull AV, Rivier CL: Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev. 1999, 79: 1-71.PubMed Turnbull AV, Rivier CL: Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev. 1999, 79: 1-71.PubMed
52.
go back to reference Doerr P, Pirke KM: Cortisol-induced suppression of plasma testosterone in normal adult males. J Clin Endocrinol Metab. 1976, 43: 622-629. 10.1210/jcem-43-3-622.PubMedCrossRef Doerr P, Pirke KM: Cortisol-induced suppression of plasma testosterone in normal adult males. J Clin Endocrinol Metab. 1976, 43: 622-629. 10.1210/jcem-43-3-622.PubMedCrossRef
53.
go back to reference Bambino TH, Hsueh AJ: Direct inhibitory effect of glucocorticoids upon testicular luteinizing hormone receptor and steroidogenesis in vivo and in vitro. Endocrinology. 1981, 108: 2142-2148. 10.1210/endo-108-6-2142.PubMedCrossRef Bambino TH, Hsueh AJ: Direct inhibitory effect of glucocorticoids upon testicular luteinizing hormone receptor and steroidogenesis in vivo and in vitro. Endocrinology. 1981, 108: 2142-2148. 10.1210/endo-108-6-2142.PubMedCrossRef
54.
go back to reference Attardi B, Tsujii T, Friedman R, Zeng Z, Roberts JL, Dellovade T, Pfaff DW, Chandran UR, Sullivan MW, DeFranco DB: Glucocorticoid repression of gonadotropin-releasing hormone gene expression and secretion in morphologically distinct subpopulations of GT1-7 cells. Mol Cell Endocrinol. 1997, 131: 241-255. 10.1016/S0303-7207(97)00102-0.PubMedCrossRef Attardi B, Tsujii T, Friedman R, Zeng Z, Roberts JL, Dellovade T, Pfaff DW, Chandran UR, Sullivan MW, DeFranco DB: Glucocorticoid repression of gonadotropin-releasing hormone gene expression and secretion in morphologically distinct subpopulations of GT1-7 cells. Mol Cell Endocrinol. 1997, 131: 241-255. 10.1016/S0303-7207(97)00102-0.PubMedCrossRef
55.
go back to reference Sapolsky RM: The influence of social hierarchy on primate health. Science. 2005, 308: 648-652. 10.1126/science.1106477.PubMedCrossRef Sapolsky RM: The influence of social hierarchy on primate health. Science. 2005, 308: 648-652. 10.1126/science.1106477.PubMedCrossRef
56.
go back to reference Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T, Sapolsky RM: Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav. 2003, 43: 67-82. 10.1016/S0018-506X(02)00037-5.PubMedCrossRef Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T, Sapolsky RM: Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav. 2003, 43: 67-82. 10.1016/S0018-506X(02)00037-5.PubMedCrossRef
57.
go back to reference Sapolsky RM: Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol. 1983, 5: 365-379. 10.1002/ajp.1350050406.CrossRef Sapolsky RM: Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol. 1983, 5: 365-379. 10.1002/ajp.1350050406.CrossRef
58.
go back to reference Muehlenbein MP, Watts DP, Whitten P: Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol. 2004, 64: 71-82. 10.1002/ajp.20062.PubMedCrossRef Muehlenbein MP, Watts DP, Whitten P: Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol. 2004, 64: 71-82. 10.1002/ajp.20062.PubMedCrossRef
59.
go back to reference Muehlenbein MP: Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am J Phys Anthropol. 2006, 130: 546-550. 10.1002/ajpa.20391.PubMedCrossRef Muehlenbein MP: Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am J Phys Anthropol. 2006, 130: 546-550. 10.1002/ajpa.20391.PubMedCrossRef
60.
go back to reference Struhsaker TT: Ecology of an African Rain Forest: Logging in Kibale and the Conflict Between Conservation and Exploitation. 1997, Gainesville: University Press of Florida Struhsaker TT: Ecology of an African Rain Forest: Logging in Kibale and the Conflict Between Conservation and Exploitation. 1997, Gainesville: University Press of Florida
61.
go back to reference Ghiglieri MP: The Chimpanzees of Kibale Forest: a Field Study of Ecology and Social Structure. 1984, New York: Columbia University Press Ghiglieri MP: The Chimpanzees of Kibale Forest: a Field Study of Ecology and Social Structure. 1984, New York: Columbia University Press
62.
go back to reference Muehlenbein MP: Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol. 2005, 65: 167-179. 10.1002/ajp.20106.PubMedCrossRef Muehlenbein MP: Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol. 2005, 65: 167-179. 10.1002/ajp.20106.PubMedCrossRef
63.
go back to reference Sousa MB, Ziegler TE: Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. Am J Primatol. 1998, 46: 105-117. 10.1002/(SICI)1098-2345(1998)46:2<105::AID-AJP1>3.0.CO;2-#.PubMedCrossRef Sousa MB, Ziegler TE: Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. Am J Primatol. 1998, 46: 105-117. 10.1002/(SICI)1098-2345(1998)46:2<105::AID-AJP1>3.0.CO;2-#.PubMedCrossRef
64.
go back to reference Milton K, Demment MW: Digestion and kinetics of passage of chimpanzees fed high and low fiber diets and comparison with human data. J Nutr. 1988, 118: 1082-1088.PubMed Milton K, Demment MW: Digestion and kinetics of passage of chimpanzees fed high and low fiber diets and comparison with human data. J Nutr. 1988, 118: 1082-1088.PubMed
65.
go back to reference Whitten PL, Brockman DK, Stavisky RC: Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yearb Phys Anthropol. 1998, 41: 1-23. 10.1002/(SICI)1096-8644(1998)107:27+<1::AID-AJPA2>3.0.CO;2-H.CrossRef Whitten PL, Brockman DK, Stavisky RC: Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yearb Phys Anthropol. 1998, 41: 1-23. 10.1002/(SICI)1096-8644(1998)107:27+<1::AID-AJPA2>3.0.CO;2-H.CrossRef
66.
go back to reference Ash LR, Orihel TC: Parasites: a Guide to Laboratory Procedures and Identification. 1987, Chicago: American Society of Clinical Pathologists Press Ash LR, Orihel TC: Parasites: a Guide to Laboratory Procedures and Identification. 1987, Chicago: American Society of Clinical Pathologists Press
67.
go back to reference Stear MJ, Bishop SC, Doligalska M, Duncan JL, Holmes PH, Irvine J, McCririe L, McKellar QA, Sinski E, Murray M: Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunol. 1995, 17: 643-652. 10.1111/j.1365-3024.1995.tb01010.x.PubMedCrossRef Stear MJ, Bishop SC, Doligalska M, Duncan JL, Holmes PH, Irvine J, McCririe L, McKellar QA, Sinski E, Murray M: Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunol. 1995, 17: 643-652. 10.1111/j.1365-3024.1995.tb01010.x.PubMedCrossRef
68.
go back to reference Decristophoris PMA, von Hardenberg A, McElligott AG: Testosterone is positively related to the output of nematode eggs in male Alpine ibex (Capra ibex) faeces. Evol Ecol Res. 2007, 9: 1277-1292. Decristophoris PMA, von Hardenberg A, McElligott AG: Testosterone is positively related to the output of nematode eggs in male Alpine ibex (Capra ibex) faeces. Evol Ecol Res. 2007, 9: 1277-1292.
70.
go back to reference Cox FEG: The parasitic protozoa and helminth worms. Infection, Resistance, and Immunity. Edited by: Kreier JP. 2002, New York: Taylor and Francis, 349-378. 2 Cox FEG: The parasitic protozoa and helminth worms. Infection, Resistance, and Immunity. Edited by: Kreier JP. 2002, New York: Taylor and Francis, 349-378. 2
71.
go back to reference Kasper LH, Buzoni-Gatel D: Ups and downs of mucosal cellular immunity against protozoan parasites. Infect Immun. 2001, 69: 1-8. 10.1128/IAI.69.1.1-8.2001.PubMedCentralPubMedCrossRef Kasper LH, Buzoni-Gatel D: Ups and downs of mucosal cellular immunity against protozoan parasites. Infect Immun. 2001, 69: 1-8. 10.1128/IAI.69.1.1-8.2001.PubMedCentralPubMedCrossRef
72.
go back to reference Rothwell TL: Immune expulsion of parasitic nematodes from the alimentary tract. Int J Parasitol. 1989, 19: 139-168. 10.1016/0020-7519(89)90003-9.PubMedCrossRef Rothwell TL: Immune expulsion of parasitic nematodes from the alimentary tract. Int J Parasitol. 1989, 19: 139-168. 10.1016/0020-7519(89)90003-9.PubMedCrossRef
73.
go back to reference King CL, Nutman TB: Biological role of helper T cell subsets in helminth infections. Regulation and Functional Significance of T-Cell Subsets. Edited by: Coffman RL. 1992, Basel: Karger, 136-155. full_text. King CL, Nutman TB: Biological role of helper T cell subsets in helminth infections. Regulation and Functional Significance of T-Cell Subsets. Edited by: Coffman RL. 1992, Basel: Karger, 136-155. full_text.
74.
go back to reference Sher A, Coffman RL: Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annu Rev Immunol. 1992, 10: 385-409. 10.1146/annurev.iy.10.040192.002125.PubMedCrossRef Sher A, Coffman RL: Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annu Rev Immunol. 1992, 10: 385-409. 10.1146/annurev.iy.10.040192.002125.PubMedCrossRef
75.
go back to reference Barrett KE, Neva FA, Gam AA, Cicmanec J, London WT, Phillips JM, Metcalfe DD: The immune response to nematode parasites: modulation of mast cell numbers and function during Strongyloides stercoralis infections in nonhuman primates. Am J Trop Med Hyg. 1988, 38: 574-581.PubMed Barrett KE, Neva FA, Gam AA, Cicmanec J, London WT, Phillips JM, Metcalfe DD: The immune response to nematode parasites: modulation of mast cell numbers and function during Strongyloides stercoralis infections in nonhuman primates. Am J Trop Med Hyg. 1988, 38: 574-581.PubMed
76.
go back to reference Urban JF, Madden KB, Svetic A, Cheever A, Trotta PP, Gause WC, Katona IM, Finkelman FD: The importance of Th2 cytokines in protective immunity to nematodes. Immunol Rev. 1992, 127: 205-220. 10.1111/j.1600-065X.1992.tb01415.x.PubMedCrossRef Urban JF, Madden KB, Svetic A, Cheever A, Trotta PP, Gause WC, Katona IM, Finkelman FD: The importance of Th2 cytokines in protective immunity to nematodes. Immunol Rev. 1992, 127: 205-220. 10.1111/j.1600-065X.1992.tb01415.x.PubMedCrossRef
77.
go back to reference Allen JE, Maizels RM: Immunology of human helminth infection. Int Arch Allergy. 1996, 109: 3-10. 10.1159/000237225. ImmunolCrossRef Allen JE, Maizels RM: Immunology of human helminth infection. Int Arch Allergy. 1996, 109: 3-10. 10.1159/000237225. ImmunolCrossRef
78.
go back to reference Else KJ, Finkelman FD: Intestinal nematode parasites, cytokines and effector mechanisms. Int J Parasitol. 1998, 28: 1145-1158. 10.1016/S0020-7519(98)00087-3.PubMedCrossRef Else KJ, Finkelman FD: Intestinal nematode parasites, cytokines and effector mechanisms. Int J Parasitol. 1998, 28: 1145-1158. 10.1016/S0020-7519(98)00087-3.PubMedCrossRef
79.
80.
go back to reference Weinstein Y, Bercovich Z: Testosterone effects on bone marrow, thymus and suppressor T cells in the (NZB × NZW) F1 mice: its relevance to autoimmunity. J Immunol. 1981, 126: 998-1002.PubMed Weinstein Y, Bercovich Z: Testosterone effects on bone marrow, thymus and suppressor T cells in the (NZB × NZW) F1 mice: its relevance to autoimmunity. J Immunol. 1981, 126: 998-1002.PubMed
81.
go back to reference Daynes RA, Araneo BA: Regulation of T-cell function by steroid hormones. Cellular and Cytokine Networks in Tissue Immunity. Edited by: Meltzer MA, Mantovani A. 1991, New York: Wiley-Liss, 77-82. Daynes RA, Araneo BA: Regulation of T-cell function by steroid hormones. Cellular and Cytokine Networks in Tissue Immunity. Edited by: Meltzer MA, Mantovani A. 1991, New York: Wiley-Liss, 77-82.
82.
go back to reference Grossman CJ, Roselle GA, Mendenhall CL: Sex steroid regulation of autoimmunity. J Steroid Biochem Mol Biol. 1991, 40: 649-659. 10.1016/0960-0760(91)90287-F.PubMedCrossRef Grossman CJ, Roselle GA, Mendenhall CL: Sex steroid regulation of autoimmunity. J Steroid Biochem Mol Biol. 1991, 40: 649-659. 10.1016/0960-0760(91)90287-F.PubMedCrossRef
83.
go back to reference Chao TC, Van Alten PJ, Walter RJ: Steroid sex hormones and macrophage function: modulation of reactive oxygen intermediates and nitrite release. Am J Reprod Immunol. 1994, 32: 43-52.PubMedCrossRef Chao TC, Van Alten PJ, Walter RJ: Steroid sex hormones and macrophage function: modulation of reactive oxygen intermediates and nitrite release. Am J Reprod Immunol. 1994, 32: 43-52.PubMedCrossRef
84.
go back to reference Grossman CJ: The role of sex steroids in immune system regulation. Bilateral Communication Between the Endocrine and Immune Systems. Edited by: Grossman CJ. 1995, New York: Springer-Verlag, 1-11. Grossman CJ: The role of sex steroids in immune system regulation. Bilateral Communication Between the Endocrine and Immune Systems. Edited by: Grossman CJ. 1995, New York: Springer-Verlag, 1-11.
85.
go back to reference Lin T, Lustig RH, Chang CF: The role of androgens-androgen receptor in immune system activity. The Physiology of Immunity. Edited by: Marsh JA, Kendall MD. 1996, New York: CRC Press, 263-276. Lin T, Lustig RH, Chang CF: The role of androgens-androgen receptor in immune system activity. The Physiology of Immunity. Edited by: Marsh JA, Kendall MD. 1996, New York: CRC Press, 263-276.
86.
go back to reference Olsen NJ, Kovacs WJ: Gonadal steroids and immunity. Endocr Rev. 1996, 17: 369-384.PubMed Olsen NJ, Kovacs WJ: Gonadal steroids and immunity. Endocr Rev. 1996, 17: 369-384.PubMed
87.
go back to reference Smithson G, Lubahn BB, Korach KS, Kincaid PW: The role of estrogen receptors and androgen receptors in sex steroid regulation of B lymphopoiesis. J Immunol. 1998, 16: 27-34. 10.1146/annurev.immunol.16.1.27.CrossRef Smithson G, Lubahn BB, Korach KS, Kincaid PW: The role of estrogen receptors and androgen receptors in sex steroid regulation of B lymphopoiesis. J Immunol. 1998, 16: 27-34. 10.1146/annurev.immunol.16.1.27.CrossRef
88.
go back to reference Straub RH, Cutolo M: Involvement of the hypothalamic-pituitary-adrenal/gonadal axis and the peripheral nervous system in rheumatoid arthritis: viewpoint based on a systemic pathogenetic role. Arthritis Rheum. 2001, 44: 493-507. 10.1002/1529-0131(200103)44:3<493::AID-ANR95>3.0.CO;2-U.PubMedCrossRef Straub RH, Cutolo M: Involvement of the hypothalamic-pituitary-adrenal/gonadal axis and the peripheral nervous system in rheumatoid arthritis: viewpoint based on a systemic pathogenetic role. Arthritis Rheum. 2001, 44: 493-507. 10.1002/1529-0131(200103)44:3<493::AID-ANR95>3.0.CO;2-U.PubMedCrossRef
89.
go back to reference Maurer M, Trajanoski Z, Frey G, Hiroi N, Galon J, Willenberg HS, Gold PW, Chrousos GP, Scherbaum WA, Bornstein SR: Differential gene expression profile of glucocorticoids, testosterone, and dehydroepiandrosterone in human cells. Horm Metab Res. 2001, 33: 691-695. 10.1055/s-2001-19142.PubMedCrossRef Maurer M, Trajanoski Z, Frey G, Hiroi N, Galon J, Willenberg HS, Gold PW, Chrousos GP, Scherbaum WA, Bornstein SR: Differential gene expression profile of glucocorticoids, testosterone, and dehydroepiandrosterone in human cells. Horm Metab Res. 2001, 33: 691-695. 10.1055/s-2001-19142.PubMedCrossRef
90.
go back to reference Wunderlich F, Benten WP, Lieberherr M, Guo Z, Stamm O, Wrehlke C, Sekeris CE, Mossmann H: Testosterone signaling in T cells and macrophages. Steroids. 2002, 67: 535-538. 10.1016/S0039-128X(01)00175-1.PubMedCrossRef Wunderlich F, Benten WP, Lieberherr M, Guo Z, Stamm O, Wrehlke C, Sekeris CE, Mossmann H: Testosterone signaling in T cells and macrophages. Steroids. 2002, 67: 535-538. 10.1016/S0039-128X(01)00175-1.PubMedCrossRef
91.
go back to reference Daynes RA, Meikle AW, Araneo BA: Locally active steroid hormones may facilitate compartmentalization of immunity by regulating the types of lymphokines produced by helper T cells. Res Immunol. 1991, 142: 40-45. 10.1016/0923-2494(91)90010-G.PubMedCrossRef Daynes RA, Meikle AW, Araneo BA: Locally active steroid hormones may facilitate compartmentalization of immunity by regulating the types of lymphokines produced by helper T cells. Res Immunol. 1991, 142: 40-45. 10.1016/0923-2494(91)90010-G.PubMedCrossRef
92.
go back to reference Huber SA, Kupperman J, Newell MK: Hormonal regulation of CD4(+) T-cell responses in coxsackievirus B3-induced myocarditis in mice. J Virol. 1999, 73: 4689-4695.PubMedCentralPubMed Huber SA, Kupperman J, Newell MK: Hormonal regulation of CD4(+) T-cell responses in coxsackievirus B3-induced myocarditis in mice. J Virol. 1999, 73: 4689-4695.PubMedCentralPubMed
93.
go back to reference Giltay EJ, Fonk JC, von Blomberg BM, Drexhage HA, Schalkwijk C, Gooren LJG: vivo effects of sex steroids on lymphocyte responsiveness and immunoglobulin levels. J Clin Endocrinol Metab. 2000, 85: 1648-1657. 10.1210/jc.85.4.1648.PubMedCrossRef Giltay EJ, Fonk JC, von Blomberg BM, Drexhage HA, Schalkwijk C, Gooren LJG: vivo effects of sex steroids on lymphocyte responsiveness and immunoglobulin levels. J Clin Endocrinol Metab. 2000, 85: 1648-1657. 10.1210/jc.85.4.1648.PubMedCrossRef
94.
go back to reference Tiuria R, Horii Y, Makimura S, Ishikawa N, Tsuchiya K, Nawa Y: Effect of testosterone on the mucosal defense against intestinal helminths in Indian soft-furred rats, Millardia meltada, with reference to goblet and mast cell responses. Parasite Immunol. 1995, 17: 479-484. 10.1111/j.1365-3024.1995.tb00918.x.PubMedCrossRef Tiuria R, Horii Y, Makimura S, Ishikawa N, Tsuchiya K, Nawa Y: Effect of testosterone on the mucosal defense against intestinal helminths in Indian soft-furred rats, Millardia meltada, with reference to goblet and mast cell responses. Parasite Immunol. 1995, 17: 479-484. 10.1111/j.1365-3024.1995.tb00918.x.PubMedCrossRef
95.
go back to reference Watanabe K, Hamano S, Noda K, Koga M, Tada I: Strongyloides ratti: additive effect of testosterone implantation and carbon injection on the susceptibility of female mice. Parasitol Res. 1999, 85: 522-526. 10.1007/s004360050591.PubMedCrossRef Watanabe K, Hamano S, Noda K, Koga M, Tada I: Strongyloides ratti: additive effect of testosterone implantation and carbon injection on the susceptibility of female mice. Parasitol Res. 1999, 85: 522-526. 10.1007/s004360050591.PubMedCrossRef
96.
go back to reference Saino N, Moller AP: Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica. Anim Behav. 1994, 48: 1325-1333. 10.1006/anbe.1994.1369.CrossRef Saino N, Moller AP: Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica. Anim Behav. 1994, 48: 1325-1333. 10.1006/anbe.1994.1369.CrossRef
97.
go back to reference Goujon E, Laye S, Parnet P, Dantzer R: Regulation of cytokine gene expression in the central nervous system by glucocorticoids: mechanisms and functional consequences. Psychoneuroendocrinology. 1997, 22: S75-S80. 10.1016/S0306-4530(97)00009-7.PubMedCrossRef Goujon E, Laye S, Parnet P, Dantzer R: Regulation of cytokine gene expression in the central nervous system by glucocorticoids: mechanisms and functional consequences. Psychoneuroendocrinology. 1997, 22: S75-S80. 10.1016/S0306-4530(97)00009-7.PubMedCrossRef
98.
go back to reference Alberts SC, Sapolsky RM, Altmann J: Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav. 1992, 26: 167-178. 10.1016/0018-506X(92)90040-3.PubMedCrossRef Alberts SC, Sapolsky RM, Altmann J: Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav. 1992, 26: 167-178. 10.1016/0018-506X(92)90040-3.PubMedCrossRef
99.
go back to reference Sapolsky RM, Spencer EM: Insulin-like growth factor I is suppressed in socially subordinate male baboons. Am J Physiol Regul Integr Comp Physiol. 1997, 273: 1346-1351. Sapolsky RM, Spencer EM: Insulin-like growth factor I is suppressed in socially subordinate male baboons. Am J Physiol Regul Integr Comp Physiol. 1997, 273: 1346-1351.
100.
go back to reference Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE: Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am J Phys Anthropol. 2006, 131: 525-534. 10.1002/ajpa.20477.PubMedCrossRef Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE: Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am J Phys Anthropol. 2006, 131: 525-534. 10.1002/ajpa.20477.PubMedCrossRef
101.
go back to reference Sapolsky RM: Social status and health in humans and other animals. Annu Rev Anthropol. 2004, 33: 393-418. 10.1146/annurev.anthro.33.070203.144000.CrossRef Sapolsky RM: Social status and health in humans and other animals. Annu Rev Anthropol. 2004, 33: 393-418. 10.1146/annurev.anthro.33.070203.144000.CrossRef
102.
go back to reference Bartoli P, Morang S, Riutort J-J, Combes C: Acquisition of parasites correlated with social rank and behavioural changes in a fish species. J Helminthol. 2000, 74: 289-293.PubMed Bartoli P, Morang S, Riutort J-J, Combes C: Acquisition of parasites correlated with social rank and behavioural changes in a fish species. J Helminthol. 2000, 74: 289-293.PubMed
103.
go back to reference Li F-H, Zhong W-Q, Want Z, Wang D-H: Rank in a food competition test and humoral immune functions in male Brandt's voles (Lasiopodomys brandtii). Physiol Behav. 2007, 90: 490-495. 10.1016/j.physbeh.2006.10.009.PubMedCrossRef Li F-H, Zhong W-Q, Want Z, Wang D-H: Rank in a food competition test and humoral immune functions in male Brandt's voles (Lasiopodomys brandtii). Physiol Behav. 2007, 90: 490-495. 10.1016/j.physbeh.2006.10.009.PubMedCrossRef
104.
go back to reference Lindstrom KM: Social status in relation in Sindbis virus infection clearance in greenfinches. Behav Ecol Sociobiol. 2004, 55: 236-241. 10.1007/s00265-003-0703-3.CrossRef Lindstrom KM: Social status in relation in Sindbis virus infection clearance in greenfinches. Behav Ecol Sociobiol. 2004, 55: 236-241. 10.1007/s00265-003-0703-3.CrossRef
105.
go back to reference Ungerfeld R, Correa O: Social dominance of female dairy goats influences the dynamics of gastrointestinal parasite eggs. Appl Anim Behav Sci. 2007, 105: 249-253. 10.1016/j.applanim.2006.05.008.CrossRef Ungerfeld R, Correa O: Social dominance of female dairy goats influences the dynamics of gastrointestinal parasite eggs. Appl Anim Behav Sci. 2007, 105: 249-253. 10.1016/j.applanim.2006.05.008.CrossRef
106.
go back to reference Hessing MJC, Scheepens CJM, Schouten WGP, Tielen MJM, Wiepkema PR: Social rank and disease susceptibility in pigs. Vet Immunol Immunopathol. 1994, 43: 373-387. 10.1016/0165-2427(94)90158-9.PubMedCrossRef Hessing MJC, Scheepens CJM, Schouten WGP, Tielen MJM, Wiepkema PR: Social rank and disease susceptibility in pigs. Vet Immunol Immunopathol. 1994, 43: 373-387. 10.1016/0165-2427(94)90158-9.PubMedCrossRef
107.
go back to reference Tuchscherer M, Puppe B, Tuchscherer A, Kanitz E: Effects of social status after mixing on immune, metabolic, and endocrine responses in pigs. Physiol Behav. 1998, 64: 353-360. 10.1016/S0031-9384(98)00084-5.PubMedCrossRef Tuchscherer M, Puppe B, Tuchscherer A, Kanitz E: Effects of social status after mixing on immune, metabolic, and endocrine responses in pigs. Physiol Behav. 1998, 64: 353-360. 10.1016/S0031-9384(98)00084-5.PubMedCrossRef
108.
go back to reference Hinson ER, Hannah MF, Norris DE, Glass GE, Klein SL: Social status does not predict responses to Seoul virus infection or reproductive success among male Norway rats. Brain Behav Immun. 2006, 20: 182-190. 10.1016/j.bbi.2005.06.003.PubMedCentralPubMedCrossRef Hinson ER, Hannah MF, Norris DE, Glass GE, Klein SL: Social status does not predict responses to Seoul virus infection or reproductive success among male Norway rats. Brain Behav Immun. 2006, 20: 182-190. 10.1016/j.bbi.2005.06.003.PubMedCentralPubMedCrossRef
109.
go back to reference Masataka N, Ishida T, Suzuki J, Matsumura S, Udono S, Sasaoka S: Dominance and immunity in chimpanzees (Pan troglodytes). Ethology. 1990, 85: 147-155. 10.1111/j.1439-0310.1990.tb00394.x.CrossRef Masataka N, Ishida T, Suzuki J, Matsumura S, Udono S, Sasaoka S: Dominance and immunity in chimpanzees (Pan troglodytes). Ethology. 1990, 85: 147-155. 10.1111/j.1439-0310.1990.tb00394.x.CrossRef
110.
go back to reference Cunnick JE, Cohen S, Rabin BS, Carpenter AB, Manuck SB, Kaplan JR: Alterations in specific antibody production due to rank and social instability. Brain Behav Immun. 1991, 5: 357-369. 10.1016/0889-1591(91)90031-5.PubMedCrossRef Cunnick JE, Cohen S, Rabin BS, Carpenter AB, Manuck SB, Kaplan JR: Alterations in specific antibody production due to rank and social instability. Brain Behav Immun. 1991, 5: 357-369. 10.1016/0889-1591(91)90031-5.PubMedCrossRef
111.
go back to reference Hausfater G, Watson DF: Social and reproductive correlates of parasite ova emissions by baboons. Nature. 1976, 262: 688-689. 10.1038/262688a0.PubMedCrossRef Hausfater G, Watson DF: Social and reproductive correlates of parasite ova emissions by baboons. Nature. 1976, 262: 688-689. 10.1038/262688a0.PubMedCrossRef
112.
go back to reference Muller-Graf CDM, Collins DA, Woolhouse MEJ: Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology. 1996, 112: 489-497. 10.1017/S0031182000076952.PubMedCrossRef Muller-Graf CDM, Collins DA, Woolhouse MEJ: Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology. 1996, 112: 489-497. 10.1017/S0031182000076952.PubMedCrossRef
113.
go back to reference Eley RM, Strum SC, Muchemi G, Reid GDF: Nutrition, body condition, activity patterns, and parasitism of free-ranging troops of olive baboons (Papio anubis) in Kenya. Am J Primatol. 1989, 18: 209-219. 10.1002/ajp.1350180304.CrossRef Eley RM, Strum SC, Muchemi G, Reid GDF: Nutrition, body condition, activity patterns, and parasitism of free-ranging troops of olive baboons (Papio anubis) in Kenya. Am J Primatol. 1989, 18: 209-219. 10.1002/ajp.1350180304.CrossRef
114.
go back to reference Schapiro SJ, Nehete PN, Perlman JE, Bloomsmith MA, Sastry KJ: Effects of dominance status and environmental enrichment on cell-mediated immunity in rhesus macaques. Appl Anim Behav Sci. 1998, 56: 319-332. 10.1016/S0168-1591(97)00087-7.CrossRef Schapiro SJ, Nehete PN, Perlman JE, Bloomsmith MA, Sastry KJ: Effects of dominance status and environmental enrichment on cell-mediated immunity in rhesus macaques. Appl Anim Behav Sci. 1998, 56: 319-332. 10.1016/S0168-1591(97)00087-7.CrossRef
115.
go back to reference Cohen S, Line S, Manuck SB, Rabin BS, Heise ER, Kaplan JR: Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med. 1997, 59: 213-221.PubMedCrossRef Cohen S, Line S, Manuck SB, Rabin BS, Heise ER, Kaplan JR: Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med. 1997, 59: 213-221.PubMedCrossRef
116.
go back to reference Ray J, Sapolsky RM: Styles of male social behavior and their endocrine correlates among high-ranking baboons. Am J Primatol. 1992, 28: 231-250. 10.1002/ajp.1350280402.CrossRef Ray J, Sapolsky RM: Styles of male social behavior and their endocrine correlates among high-ranking baboons. Am J Primatol. 1992, 28: 231-250. 10.1002/ajp.1350280402.CrossRef
117.
go back to reference Virgin CE, Sapolsky RM: Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am J Primatol. 1997, 42: 25-39. 10.1002/(SICI)1098-2345(1997)42:1<25::AID-AJP2>3.0.CO;2-0.PubMedCrossRef Virgin CE, Sapolsky RM: Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am J Primatol. 1997, 42: 25-39. 10.1002/(SICI)1098-2345(1997)42:1<25::AID-AJP2>3.0.CO;2-0.PubMedCrossRef
118.
go back to reference Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL: The effect of new alpha males on female stress in free-ranging baboons. Anim Behav. 2005, 69: 1211-1221. 10.1016/j.anbehav.2004.08.014.CrossRef Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL: The effect of new alpha males on female stress in free-ranging baboons. Anim Behav. 2005, 69: 1211-1221. 10.1016/j.anbehav.2004.08.014.CrossRef
119.
go back to reference Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL: Correlates of stress in free-ranging male chacma baboons. Anim Behav. 2005, 70: 703-713. 10.1016/j.anbehav.2004.12.017.CrossRef Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL: Correlates of stress in free-ranging male chacma baboons. Anim Behav. 2005, 70: 703-713. 10.1016/j.anbehav.2004.12.017.CrossRef
120.
go back to reference Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL: Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons. Anim Behav. 2006, 71: 1227-1237. 10.1016/j.anbehav.2005.11.009.CrossRef Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL: Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons. Anim Behav. 2006, 71: 1227-1237. 10.1016/j.anbehav.2005.11.009.CrossRef
121.
go back to reference Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL: Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas usrsinus). Proc Roy Soc Lond B. 2006, 273: 707-712. 10.1098/rspb.2005.3378.CrossRef Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL: Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas usrsinus). Proc Roy Soc Lond B. 2006, 273: 707-712. 10.1098/rspb.2005.3378.CrossRef
122.
go back to reference Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC: Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst. 2003, 34: 517-547. 10.1146/annurev.ecolsys.34.030102.151725.CrossRef Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC: Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst. 2003, 34: 517-547. 10.1146/annurev.ecolsys.34.030102.151725.CrossRef
123.
go back to reference Watts DP: Grooming between male chimpanzees at Ngogo, Kibale National Park. II. influence of male rank and possible competition for partners. Intl J Primatol. 2000, 21: 212-238. Watts DP: Grooming between male chimpanzees at Ngogo, Kibale National Park. II. influence of male rank and possible competition for partners. Intl J Primatol. 2000, 21: 212-238.
124.
go back to reference Capitanio JP, Mendoza SP, Baroncelli S: The relationship of personality dimensions in adult male rhesus macaques to progression of simian immunodeficiency virus disease. Brain Behav Immun. 1999, 13: 138-154. 10.1006/brbi.1998.0540.PubMedCrossRef Capitanio JP, Mendoza SP, Baroncelli S: The relationship of personality dimensions in adult male rhesus macaques to progression of simian immunodeficiency virus disease. Brain Behav Immun. 1999, 13: 138-154. 10.1006/brbi.1998.0540.PubMedCrossRef
125.
go back to reference Maninger N, Capitanio JP, Mendoza SP, Mason WA: Personality influences tetanus-specific antibody response in adult male rhesus macaques after removal from natal group and housing relocation. Am J Primatol. 2003, 61: 73-83. 10.1002/ajp.10111.PubMedCrossRef Maninger N, Capitanio JP, Mendoza SP, Mason WA: Personality influences tetanus-specific antibody response in adult male rhesus macaques after removal from natal group and housing relocation. Am J Primatol. 2003, 61: 73-83. 10.1002/ajp.10111.PubMedCrossRef
126.
go back to reference Coop RL, Holmes PH: Nutrition and parasite interaction. Int J Parasitol. 1996, 26: 951-962. 10.1016/S0020-7519(96)80070-1.PubMedCrossRef Coop RL, Holmes PH: Nutrition and parasite interaction. Int J Parasitol. 1996, 26: 951-962. 10.1016/S0020-7519(96)80070-1.PubMedCrossRef
127.
go back to reference Sheldon BC, Verhulst S: Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996, 11: 317-321. 10.1016/0169-5347(96)10039-2.PubMedCrossRef Sheldon BC, Verhulst S: Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996, 11: 317-321. 10.1016/0169-5347(96)10039-2.PubMedCrossRef
128.
go back to reference Gourbal BEF, Lacroix A, Gabrion C: Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. Parasitol Res. 2002, 88: 912-917. 10.1007/s00436-002-0691-7.PubMedCrossRef Gourbal BEF, Lacroix A, Gabrion C: Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. Parasitol Res. 2002, 88: 912-917. 10.1007/s00436-002-0691-7.PubMedCrossRef
129.
go back to reference Booth A, Shelley G, Mazur A, Tharp G, Kittok R: Testosterone, and winning and losing in human competition. Horm Behav. 1989, 23: 556-571. 10.1016/0018-506X(89)90042-1.PubMedCrossRef Booth A, Shelley G, Mazur A, Tharp G, Kittok R: Testosterone, and winning and losing in human competition. Horm Behav. 1989, 23: 556-571. 10.1016/0018-506X(89)90042-1.PubMedCrossRef
Metadata
Title
The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees
Authors
Michael P Muehlenbein
David P Watts
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BioPsychoSocial Medicine / Issue 1/2010
Electronic ISSN: 1751-0759
DOI
https://doi.org/10.1186/1751-0759-4-21

Other articles of this Issue 1/2010

BioPsychoSocial Medicine 1/2010 Go to the issue