Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus)

Hormones and Behavior

Volumn 62, Issue 1, 2012, Pages 27-35

  Surbeck, Martin ^a   Deschner, Tobias ^a   Weltring, Anja ^a   Hohmann, Gottfried ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

Aggression; Apes; Cortisol; Dominance status; Intersexual relationships; Mate competition; Primates

Indexed keywords

HYDROCORTISONE;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; COMPETITIVE BEHAVIOR; CONTROLLED STUDY; DOMINANCE BEHAVIOR; ESTRUS; FEMALE; HYDROCORTISONE URINE LEVEL; MALE; NONHUMAN; PAN PANISCUS; PRIORITY JOURNAL; SOCIAL BEHAVIOR; SOCIAL STATUS; WILD SPECIES;

AGGRESSION; ANIMALS; ESTRUS; FEMALE; HYDROCORTISONE; MALE; PAN PANISCUS; SOCIAL DOMINANCE;

EID: 84862247221     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.04.013     Document Type: Article

References (74)

1. Abbott D.H., Keverne E.B., Bercovitch F.B., Shively C.A., Medoza S.P., Saltzman W., Snowdon C.T., Ziegler T.E., Banjevic M., Garland T., Sapolsky R.M. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 2003, 43:67-82.
2. Alberts S.C., Altmann J., Wilson M.L. Mate guarding constrains foraging activity of male baboons. Anim. Behav. 1996, 51:1269-1277.
3. Altmann J. Observational study of behavior - sampling methods. Behaviour 1974, 49:227-267.
4. Anestis S.F. Hormones and social behavior in primates. Evol. Anthropol. 2010, 19:66-78.
5. Anestis S.F., Breakey A.A., Beuerlein M.M., Bribiescas R. Specific gravity as an alternative to creatinine for estimating urine concentration in captive and wild chimpanzee (Pan troglodytes) samples. Am. J. Primatol. 2009, 71(2):130-135.
6. Baayen R. Analyzing Linguistic Data 2008, Cambridge University Press, Cambridge.
7. Bahr N.I., Palme R., Moehle U., Hodges J.K., Heistermann M. Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen. Comp. Endocrinol. 2000, 117:427-438.
8. Bergman T.J., Beehner J.C., Cheney D.L., Seyfarth R.M., Whitten P.L. Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Anim. Behav. 2005, 70:703-713.
9. 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. Bumham K.P., Anderson D.R. Model Selection and Multimodel Inference: a Practical Information-Theoretical Approach 2002, Springer, New York. Second ed.
11. Creel S.F. Dominance, aggression, and glucocorticoid levels in social carnivores. J. Mammal. 2005, 86:255-264.
12. De Vries H.D., Netto W.J., Hanegraaf P.L.H. Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 1993, 125:157-175.
13. De Vries A.C., Glasper E.R., Detillion C.E. Social modulation of stress responses. Physiol. Behav. 2003, 79:399-407.
14. Dixson A.F. Primate Sexuality: Comparative Studies of the Monkeys, Apes and Human Beings 1998, Oxford University Press, Oxford.
15. Drews B., Harmann L.M., Beehler L.L., Bell B., Drews R.F., Hildebrandt T.B. Ultrasonographic monitoring of fetal development in unrestrained bonobos (Pan paniscus) at the Milwaukee County Zoo. Zoo Biol. 2010, 30:241-253.
16. Erb R.E., Tillson S.A., Hodgen G.D., Plotka E.D. Urinary creatinine as an index compound for estimating rate of excretion of steroids in the domestic sow. J. Anim. Sci. 1970, 30:79-85.
17. Fichtel C., Kraus C., Ganswindt A., Heistermann M. Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Horm. Behav. 2007, 51:640-648.
18. Forstmeier W., Schielzeth H. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. Behav. Ecol. Sociobiol. 2011, 65:47-55.
19. Fruth B., Hohmann G. How bonobos handle hunts and harvests: why share food?. Behavioural Diversity in Chimpanzees and Bonobos 2002, 231-243. Cambridge University Press, Cambridge. C. Boesch, G. Hohmann, L. Vigilant (Eds.).
20. Furuichi T. Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba, Zaire. Int. J. Primatol. 1997, 18:855-875.
21. Furuichi T., Hashimoto C. Why female bonobos have a lower copulation rate during estrus than chimpanzees. Behavioural Diversity in Chimpanzees and Bonobos 2002, 156-167. Cambridge University Press, Cambridge. C. Boesch, G. Hohmann, L. Vigilant (Eds.).
22. Furuichi T., Ihobe H. Variation in male relationships in bonobos and chimpanzees. Behaviour 1994, 130:211-228.
23. Furuichi T., Idani G., Ihobe H., Kuroda S., Kitamura K., Mori A., Enomoto T., Okayasu N., Hashimoto C., Kano T. Population dynamics of wild bonobos (Pan paniscus) at Wamba. Int. J. Primatol. 1998, 19:1029-1044.
24. Gesquiere L.R., Learn N.H., Simao C.M., Onyango P.O., Alberts S.C., Altmann J. Life at the top: rank and stress in wild male baboons. Science 2011, 333:357-360.
25. Goymann W., Wingfield J.C. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 2004, 67:591-602.
26. Goymann W., East M.L., Wachter B., Honer O.P., Mostl E., Hofer H. Defense of females, but not social status, predicts plasma androgen levels in male spotted hyenas. Physiol. Biochem. Zool. 2003, 76:586-593.
27. Hauser B., Deschner T., Boesch C. Development of a liquid chromatography-tandem mass spectrometry method for the determination of 23 endogenous steroids in small quantities of primate urine. J. Chromatogr. B 2008, 862:100-112.
28. Hauser B., Schulz D., Boesch C., Deschner T. Measuring urinary testosterone levels of the great apes - problems with enzymatic hydrolysis using Helix pomatia juice. Gen. Comp. Endocrinol. 2008, 158:77-86.
29. Hohmann G., Fruth B. Use and function of genital contacts among female bonobos. Anim. Behav. 2000, 60:107-120.
30. Hohmann G., Fruth B. Intra- and inter-sexual aggression by bonobos in the context of mating. Behaviour 2003, 140:1389-1413.
31. Hohmann G., Fruth B. Lui Kotal - a new site for field research on bonobos in the Salonga National Park. Pan Afr. News 2003, 10:25-27.
32. Hohmann G., Mundry R., Deschner T. The relationship between socio-sexual behavior and salivary cortisol in bonobos: tests of the tension regulation hypothesis. Am. J. Primatol. 2009, 71:223-232.
33. Kano T. The Last Ape: Pygmy Chimpanzee Behavior and Ecology 1992, Stanford University Press, Stanford, CA.
34. Koren L., Mokady O., Geffen E. Social status and cortisol levels in singing rock hyraxes. Horm. Behav. 2008, 54:212-216.
35. Lynch J.W., Ziegler T.E., Strier K.B. Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm. Behav. 2002, 41:275-287.
36. Marshall A.J., Hohmann G. Urinary testosterone levels of wild male bonobos (Pan paniscus) in the Lomako Forest, Democratic Republic of Congo. Am. J. Primatol. 2005, 65:87-92.
37. Massé R., Ayotte C., Dugal R. Studies on anabolic steroids: I. Integrated methodological approach to the gas chromatographic-mass spectrometric analysis of anabolic steroid metabolites in urine. J. Chromatogr. B Biomed. Sci. Appl. 1989, 489:23-50.
38. McEwen B.S., Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 2003, 43:2-15.
39. Messeri G., Cugnetto G., Moneti G., Serio M. Helix pomatia induced conversion of some 3[beta]-hydroxysteroids. J. Steroid Biochem. 1984, 20:793-796.
40. Mooring M.S., Patton M.L., Lance V.A., Hall B.M., Schaad E.W., Fetter G.A., Fortin S.S., McPeak K.M. Glucocorticoids of bison bulls in relation to social status. Horm. Behav. 2006, 49:369-375.
41. Muller M. 2002. Endocrine aspects of aggression and dominance in chimpanzees of the Kibale Forest. Ph.D. thesis. University of Southern California.
42. Muller M.N. Dominance, cortisol and stress, in wild chimpanzees. Am. J. Phys. Anthropol. 2004, (Suppl. 151).
43. Muller M.N., Mitani J.C. Conflict and cooperation in wild chimpanzees. Advances in the Study of Behavior 2005, 275-331. Academic Press.
44. Muller M.N., Wrangham R.W. Dominance, aggression and testosterone in wild chimpanzees: a test of the 'challenge hypothesis'. Anim. Behav. 2004, 67:113-123.
45. Muller M.N., Wrangham R.W. Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 2004, 55:332-340.
46. Mundry R., Nunn C.L. Stepwise model fitting and statistical inference: turning noise into signal pollution. Am. Nat. 2009, 173:119-123.
47. Nishida T. Alpha status and agonistic alliance in wild chimpanzees (Pan troglodytes schweinfurthii). Primates 1983, 24:318-336.
48. Ostner J., Heistermann M., Schülke O. Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm. Behav. 2008, 54:613-619.
49. Ostner J., Kappeler P., Heistermann M. Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 2008, 62:627-638.
50. Paoli T. The absence of sexual coercion in bonobos. Sexual Coercion in Primates and Humans 2009, 410-423. Harvard University Press, Cambridge. M.N. Muller, R.W. Wrangham (Eds.).
51. Parish A.R. Female relationships in bonobos (Pan paniscus) - evidence for bonding, cooperation, and female dominance in a male-philopatric species. Hum. Nature-Int. Bios. 1996, 7:61-96.
52. Sands J., Creel S. Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim. Behav. 2004, 67:387-396.
53. Sapolsky R.M. The endocrine stress-response and social status in the wild baboon. Horm. Behav. 1982, 16:279-292.
54. Sapolsky R.M. Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am. J. Primatol. 1986, 11:217-227.
55. Sapolsky R.M. The physiology of dominance in stable versus unstable hierarchies. Primate Social Conflict 1993, State University of New York Press, Albany. W.A. Mason, S.P. Mendoza (Eds.).
56. Sapolsky R.M. Endocrinology of the stress response. Behavioural Endocrinology 2002, 409-450. MIT Press, Cambridge. J. Becker (Ed.).
57. Setchell J.M., Dixson A.F. Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm. Behav. 2001, 39:177-184.
58. Setchell J.M., Charpentier M., Wickings E.J. Mate guarding and paternity in mandrills: factors influencing alpha male monopoly. Anim. Behav. 2005, 70:1105-1120.
59. Setchell J.M., Smith T., Wickings E.J., Knapp L.A. Stress, social behaviour, and secondary sexual traits in a male primate. Horm. Behav. 2010, 58:720-728.
60. Stumpf R.M. Chimpanzees and bonobos: diversity within and between species. Primates in Perspective 2007, 321-344. Oxford University Press, Oxford. C.J. Campbell (Ed.).
61. Surbeck M., Mundry R., Hohmann G. Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 278:590-598.
62. Surbeck M., Deschner T., Schubert G., Weltring A., Hohmann G. Anim. Behav. 2012, 83:659-669.
63. Takahata Y., Ihobe H., Idani G. Comparing copulations of chimpanzees and bonobos: do females exhibit proceptivity or receptivity?. Great Ape Societies 1996, 146-155. Cambridge University Press, Cambridge. W. McGrew, L. Marchant, T. Nishida (Eds.).
64. Takahata Y., Ihobe H., Idani G. Do bonobos copulate more frequently and promiscuously than chimpanzees?. Hum. Evol. 1999, 14:159-167.
65. Van Belle S., Ziegler T.E., Estrada A., Strier K.B. Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra). Am. J. Phys. Anthropol. 2009, 260.
66. van de Pol M.V., Wright J. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 2009, 77:753-758.
67. van der Meij L., Buunk A.P., Salvador A. Contact with attractive women affects the release of cortisol in men. Horm. Behav. 2010, 58:501-505.
68. Venturelli E., Cavalleri A., Secreto G. Methods for urinary testosterone analysis. J. Chromatogr. B Biomed. Sci. Appl. 1995, 671:363-380.
69. Vervaecke H., de Vries H., van Elsacker L. Dominance and its behavioral measures in a captive group of bonobos (Pan paniscus). Int. J. Primatol. 2000, 21:47-68.
70. Weingrill T., et al. Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm. Behav. 2004, 45:259-269.
71. Whittingham M.J., Stephens P.A., Bradbury R.B., Freckleton R.P. Why do we still use stepwise modelling in ecology and behaviour?. J. Anim. Ecol. 2006, 75:1182-1189.
72. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 2003, 15:711-724.
73. Wobber V., Hare B., Maboto J., Lipson S., Wrangham R., Ellison P.T. Differential changes in steroid hormones before competition in bonobos and chimpanzees. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:12457-12462.
74. Wrangham R.W., Peterson D. Demonic Males 1996, Houghton Mifflin, New York.