Individual variation and the endocrine regulation of behaviour and physiology in birds: A cellular/molecular perspective

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1497, 2008, Pages 1699-1710

  Ball, Gregory F ^a,b   Balthazart, Jacques ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Oestrogen receptor; Sex differences; Steroid hormones

Indexed keywords

BIRD; ECOPHYSIOLOGY; ENDOCRINE SYSTEM; ESTROGENIC COMPOUND; GENETIC ANALYSIS; HORMONE; INDIVIDUAL VARIATION; STEROID;

AVES; VERTEBRATA;

EID: 41149107024     PISSN: 09628452     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.0010     Document Type: Review

References (100)

1. Absil, P., Braquenier, J. B., Balthazart, J. & Ball, G. F. 2002 Effects of lesions of nucleus taeniae on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Brain Behav. Evol. 60, 13-35. (doi:10.1159/000064119)
2. Adkins, E. K. 1975 Hormonal basis of sexual differentiation in the Japanese quail. J. Comp. Physiol. Psychol. 89, 61-71. (doi:10.1037/h0076406)
3. Adkins-Regan, E. 2005 Hormones and animal social behavior. Princeton, NJ: Princeton University Press.
4. Arnold, A. P. 1975 The effects of castration and androgen replacement on song courtship, and aggression in zebra finches (Poephila guttata). J. Exp. Zool. 191, 309-326. (doi:10.1002/jez.1401910302)
5. Arnold, A. P. 1992 Developmental plasticity in neural circuits controlling birdsong: sexual differentiation and the neural basis of learning. J. Neurobiol. 23, 1506-1528. (doi:10.1002/neu.480231010)
6. Arnold, A. P. & Saltiel, A. 1979 Sexual difference in pattern of hormone accumulation in the brain of a song bird. Science 205, 702-705. (doi:10.1126/science.205.4407.702)
7. Auger, C. J., Bentley, G. E., Auger, A. P., Ramamurthy, M. & Ball, G. F. 2002 Expression of cAMP response element binding protein-binding protein in the song control system and hypothalamus of adult european starlings (Sturnus vulgaris). J. Neuroendocrinol. 14, 805-813. (doi:10.1046/j.1365- 2826.2002.00842.x)
8. Ball, G. F. & Balthazart, J. 2002 Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. In Hormones, brain and behavior, vol. 2 (eds D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach & R. T. Rubin), pp. 649-798. San Diego, CA: Academic Press.
9. Ball, G. F., Riters, L. V. & Balthazart, J. 2002 Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front. Neuroendocrinol. 23, 137-178. (doi:10.1006/frne.2002.0230)
10. Ball, G. F., Castelino, C. B., Maney, D. L., Appeltants, D. & Balthazart, J. 2003 The activation of birdsong by testosterone: multiple sites of action and role of ascending catecholamine projections. Ann. NY Acad. Sci. 1007, 211-231. (doi:10.1196/annals.1286.021)
11. Ball, G. F., Auger, C. J., Bernard, D. J., Charlier, T. D., Sartor, J. J., Riters, L. V. & Balthazart, J. 2004 Seasonal plasticity in the song control system. Multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann. NY Acad. Sci. 1016, 586-610. (doi:10.1196/annals.1298.043)
12. Balthazart, J. 1983 Hormonal correlates of behavior. In Avian biology, vol. VII (eds D. S. Farner, J. R. King & K. C. Parkes), pp. 221-365. New York, NY: Academic Press.
13. Balthazart, J. 1989 Steroid metabolism and the activation of social behavior. In Advances in comparative and environmental physiology, vol. 3 (ed. J. Balthazart), pp. 105-159. Berlin, Germany: Springer.
14. Balthazart, J. & Ball, G. F. 2006 Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci. 29, 241-249. (doi:10.1016/j.tins.2006.03.004)
15. Balthazart, J. & Hendrick, J. C. 1976 Annual variation in reproductive behavior, testosterone, and plasma FSH levels in the Rouen duck, Anas platyrhynchos. Gen. Comp. Endocrinol. 28, 171-183. (doi:10.1016/0016-6480(76)90169-6)
16. Balthazart, J. & Hendrick, J. C. 1979 Effects of exogenous gonadotropic and steroid hormones on the social behaviour and gonadal maturation of male domestic ducks. Arch. Int. Physiol. Biochem. 87, 741-761.
17. Balthazart, J. & Schumacher, M. 1985 Role of testosterone metabolism in the activation of sexual behaviour in birds. In Neurobiology, current comparative approaches (eds R. Gilles & J. Balthazart), pp. 121-140. Berlin, Germany: Springer.
18. Balthazart, J. & Stevens, M. 1975 Effects of testosterone propionate on the social behaviour of groups of male comestic ducklings Anas platyrhynchos L. Anim. Behav. 23, 926-931. (doi:10.1016/0003-3472(75)90116-5)
19. Balthazart, J. & Surlemont, C. 1990 Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol. Behav. 48, 599-609. (doi:10.1016/0031-9384(90)90198-D)
20. Balthazart, J., Deviche, P. & Hendrick, J. C. 1977 Effects of exogenous hormones on the reproductive behaviour of adult male domestic ducks. II Correlation with morphology and hormone plasma levels. Behav. Process. 2, 147-161. (doi:10.1016/0376-6357(77)90017-1)
21. Balthazart, J., Massa, R. & Negri-Cesi, P. 1979 Photoperiodic control of testosterone metabolism, plasma gonadotrophins, cloacal gland growth, and reproductive behavior in the Japanese quail. Gen. Comp. Endocrinol. 39, 222-235. (doi:10.1016/0016-6480(79)90227-2)
22. Balthazart, J., Schumacher, M. & Ottinger, M. A. 1983 Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen. Comp. Endocrinol. 51, 191-207. (doi:10.1016/0016-6480(83)90072-2)
23. Balthazart, J., Gahr, M. & Surlemont, C. 1989 Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study. Brain Res. 501, 205-214. (doi:10.1016/0006-8993(89)90638-0)
24. Balthazart, J., Foidart, A. & Hendrick, J. C. 1990 The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 47, 83-94. (doi:10.1016/0031-9384(90)90045-6)
25. Balthazart, J., Tlemçani, O. & Ball, G. F. 1996 Do sex differences in the brain explain sex differences in the hormonal induction of reproductive behavior? What 25 years of research on the Japanese quail tells us. Horm. Behav. 30, 627-661. (doi:10.1006/hbeh.1996.0066)
26. Balthazart, J., Baillien, M., Cornil, C. A. & Ball, G. F. 2004 Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol. Behav. 83, 247-270. (doi:10.1016/j.physbeh.2004. 08.025)
27. Barfield, R. J. 1971 Activation of sexual and aggressive behavior by androgen implantation into the male ring dove brain. Endocrinology 89, 1470-1476.
28. Benoff, F. H., Siegel, P. B. & Van Krey, H. P. 1978 Testosterone determinations in lines of chickens selected for differential mating frequency. Horm. Behav. 10, 246-250. (doi:10.1016/0018-506X(78)90068-5)
29. Bernard, D. J., Bentley, G. E., Balthazart, J., Turek, F. W. & Ball, G. F. 1999 Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology 140, 4633-4643. (doi:10.1210/en.140.10.4633)
30. Berthold, A. A. 1849 Transplantation der Hoden. Arch. Anat. Physiol. 16, 42-46.
31. Blaustein, J. D. & Olster, D. H. 1989 Gonadal steroid hormone receptors and social behaviors. In Advances in comparative and environmental physiology, vol. 3 (ed. J. Balthazart), pp. 31-104. Berlin, Germany: Springer.
32. Brenowitz, E. A. & Arnold, A. P. 1992 Hormone accumulation in song regions of the canary brain. J. Neurobiol. 23, 871-880. (doi:10.1002/neu.480230708)
33. Breuner, C. W. & Orchinik, M. 2002 Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175, 99-112. (doi:10.1677/joe.0.1750099)
34. Breuner, C. W., Lynn, S. E., Julian, G. E., Cornelius, J. M., Heidinger, B. J., Love, O. P., Sprague, R. S., Wada, H. & Whitman, B. A. 2006 Plasma-binding globulins and acute stress response. Horm. Metab. Res. 38, 260-268. (doi:10.1055/s-2006-925347)
35. Carere, C. & Balthazart, J. 2007 Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol. Metab. 18, 73-80. (doi:10.1016/j.tem.2007.01.003)
36. Charlier, T. D., Lakaye, B., Ball, G. F. & Balthazart, J. 2002 Steroid receptor coactivator SRC-1 exhibits high expression in steroid-sensitive brain areas regulating reproductive behaviors in the quail brain. Neuroendocrinology 76, 297-315. (doi:10.1159/000066624)
37. Charlier, T. D., Balthazart, J. & Ball, G. F. 2003 Sex differences in the distribution of the steroid receptor coactivator SRC-1 in the song control nuclei of male and female canaries. Brain Res. 959, 263-274. (doi:10.1016/S0006-8993(02)03758-7)
38. Charlier, T. D., Ball, G. F. & Balthazart, J. 2005 Inhibition of steroid receptor coactivator-1 blocks estrogen and androgen action on male sex behavior and associated brain plasticity. J. Neurosci. 25, 906-913. (doi:10.1523/JNEUROSCI.3533-04.2005)
39. Charlier, T. D., Ball, G. F. & Balthazart, J. 2006 Plasticity in the expression of the steroid receptor coactivator 1 in the Japanese quail brain: effect of sex, testosterone, stress and time of the day. Neuroscience 140, 1381-1394. (doi:10.1016/j.neuroscience.2006.03.002)
40. Cheng, M. F., Chaiken, M., Zuo, M. & Miller, H. 1999 Nucleus taenia of the amygdala of birds: anatomical and functional studies in ring doves (Streptopelia risoria) and European starlings (Sturnus vulgaris). Brain Behav. Evol. 53, 243-270. (doi:10.1159/000006597)
41. Clayton, D. F. 2004 Songbird genomics: methods, mechanisms, opportunities, and pitfalls. Ann. NY Acad. Sci. 1016, 45-60. (doi:10.1196/annals.1298.028)
42. Cohen-Parsons, M., Van Krey, H. P. & Siegel, P. B. 1983 In vivo aromatization of [3H] testosterone in high and low mating lines of Japanese quail. Horm. Behav. 17, 316-323. (doi:10.1016/0018- 506X(83)90031-4)
43. Cornil, C. A., Ball, G. F. & Balthazart, J. 2006 Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res. 1126, 2-26. (doi:10.1016/j. brainres.2006.07.098)
44. Crews, D. 1998 On the organization of individual difference in sexual behavior. Am. Zool. 38, 118-132.
45. Cunningham, D. L., Siegel, P. B. & Van Krey, H. P. 1977 Androgen influence on mating behavior in selected lines of Japanese quail. Horm. Behav. 8, 166-174. (doi:10.1016/0018-506X(77)90033-2)
46. Damassa, D. A., Smith, E. R., Tennent, B. & Davidson, J. M. 1977 The relationship between circulating testosterone levels and male sexual behavior in rats. Horm. Behav. 8, 275-286. (doi:10.1016/0018-506X(77)90002-2)
47. Delville, Y., Hendrick, J. C., Sulon, J. & Balthazart, J. 1984 Testosterone metabolism and testosterone-dependent characteristics in Japanese quail. Physiol. Behav. 33, 817-823. (doi:10.1016/0031-9384(84) 90053-2)
48. Desjardins, C. & Turek, F. W. 1977 Effects of testosterone on spermatogenesis and luteinizing hormone release in Japanese quail. Gen. Comp. Endocrinol. 33, 293-303. (doi:10.1016/0016-6480(77)90253-2)
49. Dessi-Fulgheri, F., Lucarini, N. & Lupo di Prisco, C. 1976 Relationships between testosterone metabolism in the brain, other endocrine variables and intermale aggression in mice. Aggr. Behav. 2, 223-231. (doi:10.1002/1098-2337(1976)2:3〈223::AID-AB2480020307〉3.0. CO;2-0)
50. Deviche, P. 1979 Behavioral effects of castration and tesosterone propionate replacement combined with ACTH in the male domestic duck (Anas platyrhynchos L.). J. Exp. Zool. 207, 471-480. (doi:10.1002/jez.1402070315)
51. Deviche, P., Breuner, C. & Orchinik, M. 2001 Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. Gen. Comp. Endocrinol. 122, 67-77. (doi:10.1006/gcen.2001.7613)
52. Feder, H. H. 1984 Hormones and sexual behavior. Ann. Rev. Psychol. 1984, 165-200. (doi:10.1146/annurev.ps.35.020184.001121)
53. Fidler, A. E., van Oers, K., Drent, P. J., Kuhn, S., Meuller, J. C. & Kempaenaers, B. 2007 Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc. R. Soc. B 274, 1685-1691. (doi:10.1098/rspb.2007.0337)
54. Foidart, A., Lakaye, B., Grisar, T., Ball, G. F. & Balthazart, J. 1999 Estrogen receptor-beta in quail: cloning, tissue expression and neuroanatomical distribution. J. Neurobiol. 40, 327-342. (doi:10.1002/(SICI)1097-4695(19990905)40:3〈327::AID-NEU5〉3.0.CO;2-L)
55. Fusani, L. & Gahr, M. 2006 Hormonal influence on song structure and organization: the role of estrogen. Neuroscience 138, 939-946. (doi:10.1016/j.neuroscience.2005.08.041)
56. Goymann, W., Landys, M. M. & Wingfield, J. C. 2007 Distinguishing seasonal androgen responses from male-male androgen responsiveness - revisiting the challenge hypothesis. Horm. Behav. 51, 463-476. (doi:10.1016/j.yhbeh.2007.01.007)
57. Groothuis, T. G. & Carere, C. 2005 Avian personalities: characterization and epigenesis. Neurosci. Biobehav. Rev. 29, 137-150. (doi:10.1016/j.neubiorev.2004.06.010)
58. Grunt, J. A. & Young, W. C. 1952 Differential reactivity of individuals and the response of the male guinea pig to testosterone propionate. Endocrinology 51, 237-248.
59. Hammond, G. L. 1995 Potential function of plasma steroidbinding proteins. Trends Endocrinol. Metab. 6, 298-304. (doi:10.1016/1043-2760(95) 00162-X)
60. Hammond, G. L. 2002 Access of reproductive steroids to target tissues. Obstet. Gynecol. Clin. North Am. 29, 411-423. (doi:10.1016/S0889- 8545(02)00008-6)
61. Harding, C. F., Sheridan, K. & Walters, M. J. 1983 Hormonal specificity and activation of sexual behavior in male zebra finches. Horm. Behav. 17, 111-133. (doi:10.1016/0018-506X(83)90021-1)
62. Harding, C. F., Walters, M. J., Collado, D. & Sheridan, K. 1988 Hormonal specificity and activation of social behavior in male red-winged blackbirds. Horm. Behav. 22, 402-418. (doi:10.1016/0018-506X(88) 90011-6)
63. Herbert, Z., Pollak, E., Caldwell, J. D. & Jirikowski, G. F. 2003 Subcellular localization of sex hormone-binding globulin/SHBG in rat hypothalamus and pituitary. Abstr. Soc. Neurosci., 29.
64. Herbert, Z., Gothe, S., Caldwell, J. D., Bernstein, H. G., Melle, C., Von Eggeling, F., Lewis, J. & Jirikowski, G. F. 2005 Identification of sex hormone-binding globulin in the human hypothalamus. Neuroendocrinology 81, 287-293. (doi:10.1159/000088170)
65. Hews, D. K. & Moore, M. C. 1997 Hormones and sex-specific traits: critical questions. In Parasites and pathogens: effects on host hormones and behavior (ed. N. E. Beckage), pp. 277-292. New York, NY: International Thomas Publisher.
66. Hutchison, J. B. 1970 Differential effects of testosterone and oestradiol on male courtship behaviour in the Barbary dove (Streptopelia risoria). Anim. Behav. 18, 41-51. (doi:10.1016/0003-3472(70)90068-0)
67. Hutchison, J. B. 1971 Effects of hypothalamic implants of gonadal steroids on courtship behaviour in Barbary doves (Streptopelia risoria). J. Endocrinol. 50, 97-113.
68. Kuiper, G. G. J. M., Enmark, E., Pelto-Huikko, M., Nilsson, S. & Gustafsson, J. Å. 1996 Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl Acad. Sci. USA 93, 5925-5930. (doi:10.1073/pnas.93.12.5925)
69. MacDougall-Shackleton, S. A. & Ball, G. F. 1999 Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci. 22, 432-436. (doi:10.1016/S0166-2236(99)01434-4)
70. Maley, M. J. 1969 Electrical stimulation of agonistic behavior in the mallard. Behaviour 34, 138-160.
71. McCollom, R. E., Siegel, P. B. & Van Krey, H. P. 1971 Responses to androgen in lines of chickens selected for mating behavior. Horm. Behav. 2, 31-42. (doi:10.1016/0018-506X(71)90035-3)
72. McEwen, B. S. 2001 Genome and hormones: gender differences in physiology - invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J. Appl. Physiol. 91, 2785-2801.
73. McEwen, B. S. & Alves, S. E. 1999 Estrogen actions in the central nervous system. Endocr. Rev. 20, 279-307. (doi:10.1210/er.20.3. 279)
74. McKenna, N. J. & O'Malley, B. W. 2000 From ligand to response: generating diversity in nuclear receptor coregulator function. J. Steroid Biochem. Mol. Biol. 74, 351-356. (doi:10.1016/S0960-0760(00)00112-6)
75. McKenna, N. J. & O'Malley, B. W. 2002 Minireview: nuclear receptor coactivators - an update. Endocrinology 143, 2461-2465. (doi:10.1210/en.143.7.2461)
76. McKenna, N. J., Lanz, R. B. & O'Malley, B. W. 1999 Nuclear receptor coregulators: cellular and molecular biology. Endocr. Rev. 20, 321-344. (doi:10.1210/er.20.3.321)
77. Morrell, J. I. & Pfaff, D. W. 1978 A neuroendocrine approach to brain function: localization of sex steroid concentrating cells in vertebrate brains. Am. Zool. 18, 447-460.
78. Nettle, D. 2006 The evolution of personality variation in humans and other animals. Am. Psychol. 61, 622-631. (doi:10.1037/0003-066X. 61.6.622)
79. Pfaff, D. W. 1999 Drive. Neurobiological and molecular mechanisms of sexual motivation. Cambridge, MA: The MIT Press.
80. Pfaff, D. W. & Pfaffmann, C. 1969 Olfactory and hormonal influences on the basal forebrain of the male rat. Brain Res. 15, 137-156. (doi:10.1016/0006-8993(69)90315-1)
81. Pfaff, D. W., Phillips, M. I. & Rubin, R. T. 2004 Principles of hormone/behavior relations. Amsterdam, The Netherlands: Elsevier.
82. Phillips, R. E. 1964 Wildness in the mallard duck. Effects of brain lesions and stimulation on escape behavior and reproduction. J. Comp. Neurol. 122, 139-155. (doi:10.1002/cne.901220202)
83. Portillo, W., Castillo, C. G., Retana-Marquez, S., Roselli, C. E. & Paredes, R. G. 2007 Neuronal activity of aromatase enzyme in non-copulating male rats. J. Neuroendocrinol. 19, 139-141. (doi:10.1111/j.1365-2826. 2006.01513.x)
84. Ramenofsky, M. 1984 Agonistic behaviour and endogenous plasma hormones in male japanese quail. Anim. Behav. 32, 698-708. (doi:10.1016/S0003-3472(84)80145-1)
85. Reiner, A. D. et al. 2004 Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377-414. (doi:10.1002/cne.20118)
86. Schumacher, M. & Balthazart, J. 1983 The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol. Behav. 30, 335-339. (doi:10.1016/0031-9384(83) 90135-X)
87. Schumacher, M. & Balthazart, J. 1986 Testosterone-induced brain aromatase is sexually dimorphic. Brain Res. 370, 285-293. (doi:10.1016/0006-8993(86)90483-X)
88. Sisneros, J. A., Forlano, P. M., Dietcher, D. L. & Bass, A. H. 2004 Steroid-dependent plasticity leads to adaptive coupling of sender and receiver. Science 305, 404-407. (doi:10.1126/science.1097218)
89. Thompson, R. R., Goodson, J. L., Ruscio, M. G. & Adkins-Regan, E. 1998 Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals. Brain Behav. Evol. 51, 215-229. (doi:10.1159/000006539)
90. Tsai, M. J. & O'Malley, B. W. 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63, 451-486. (doi:10.1146/annurev.bi.63.070194.002315)
91. Tsutsui, K. & Ishii, S. 1981 Effects of sex steroids on agressive behavior of adult male japanese quail. Gen. Comp. Endocrinol. 44, 480-486. (doi:10.1016/0016-6480(81)90336-1)
92. Turek, F. W., Desjardins, C. & Menaker, M. 1976 Antigonadal and progonadal effects of testosterone in male house sparrows. Gen. Comp. Endocrinol. 28, 395-402. (doi:10.1016/0016-6480(76)90147-7)
93. Van Krey, H. P., Siegel, P. B., Balander, R. J. & Benoff, F. H. 1983 Testosterone aromatization in high and low mating lines of Gallinaceous birds. Physiol. Behav. 31, 153-157. (doi:10.1016/0031-9384(83)90112-9)
94. Voigt, C., Ball, G.F. & Balthazart, J. 2007 Sex differences in the expression of sex steroid receptors mRNA in the quail brain, Abst. 209.21/HHH26 of the Soc. for Neurosci. Meeting.
95. Walters, M. J. & Harding, C. F. 1988 The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches. Horm. Behav. 22, 207-218. (doi:10.1016/0018-506X(88)90067-0)
96. Wang, Y. M., Bayliss, D. A., Millhorn, D. E., Petrusz, P. & Joseph, D. R. 1990 The androgen-binding protein gene is expressed in male and female rat brain. Endocrinology 127, 3124-3130.
97. Watson, J. T. & Adkins-Regan, E. 1989 Neuroanatomical localization of sex steroid-concentrating cells in the Japanese quail (Coturnix japonica): autoradiography with [3H]-testosterone, [3H]-estradiol, and [3H]-dihydrotestosterone. Neuroendocrinology 49, 51-64.
98. Wingfield, J. & Ramenofsky, M. 1985 Testosterone and aggressive behaviour during the reproductive cycle of male birds. In Comparative neurobiology (ed. J. Balthazart), pp. 93-104. Berlin, Germany: Springer.
99. Wingfield, J. C. & Silverin, B. 2002 Ecophysiological studies of hormone-behavior relations in birds. In Hormones, brain and behavior, vol. 2 (eds D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach & R. T. Rubin), pp. 587-648. Amsterdam, The Netherlands: Elservier.
100. Wingfield, J. C., Hegner, R. E., Dufty, A. M. & Ball, G. F. 1990 The challenge hypothesis - theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am. Nat. 136, 829-846. (doi:10.1086/285134)