Regulation of plasma testosterone, corticosterone, and metabolites in response to stress, reproductive stage, and social challenges in a desert male songbird

General and Comparative Endocrinology

Volumn 203, Issue , 2014, Pages 120-131

  Deviche, Pierre ^a   Beouche Helias, Benjamin ^b   Davies, Scott ^a   Gao, Sisi ^a   Lane, Samuel ^a   Valle, Shelley ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITÉ DE POITIERS   (France)

Author keywords

Challenge hypothesis; Glycemia; Reproduction; Simulated territorial intrusion; Song playback; Uric acid

Indexed keywords

CORTICOSTERONE; GLUCOSE; TESTOSTERONE; URIC ACID;

ACUTE STRESS; ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BODY MASS; BREEDING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FEATHER; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; LONG TERM EXPOSURE; MALE; METABOLIC REGULATION; MOLTING; NONHUMAN; PEUCAEA CARPALIS; PRIORITY JOURNAL; SEASONAL VARIATION; SOCIAL BEHAVIOR; SPARROW; SUMMER; TERRITORIALITY; TESTOSTERONE BLOOD LEVEL; URIC ACID BLOOD LEVEL; VISUAL STIMULATION; AGGRESSION; ANIMAL; BLOOD; DESERT CLIMATE; EXERCISE; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REPRODUCTION; SEASON; SEXUAL BEHAVIOR; SONGBIRD;

AGGRESSION; ANIMALS; CORTICOSTERONE; DESERT CLIMATE; MALE; MOLTING; REPRODUCTION; RESTRAINT, PHYSICAL; SEASONS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; SONGBIRDS; STRESS, PSYCHOLOGICAL; TERRITORIALITY; TESTOSTERONE;

EID: 84906794596     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2014.01.010     Document Type: Article

References (89)

1. Alonso-Alvarez C., Ferrer M. A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol. Biochem. Zool. 2001, 74:703-713.
2. Anthony N.B., Vasilatos-Younken R., Bacon W.L., Lilburn M.S. Secretory pattern of growth hormone, insulin, and related metabolites in growing male turkeys: effects of overnight fasting and refeeding. Poult. Sci. 1990, 69:801-811.
3. Apfelbeck B., Goymann W. Ignoring the challenge? Male black redstarts (Phoenicurus ochruros) do not increase testosterone levels during territorial conflicts but they do so in response to gonadotropin-releasing hormone. Proc. Biol. Sci. 2011, 278:3233-3242.
4. Austin T., Ricklefs E. Growth and development of the Rufous-winged Sparrow (Aimophila carpalis). Condor 1977, 79:37-50.
5. Belo P.S., Romsos D.R., Leville G.A. Blood metabolites and glucose metabolism in the fed and fasted chicken. J. Nutr. 1976, 106:1135-1143.
6. Braun E.J., Sweazea K.L. Glucose regulation in birds. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 151:1-9.
7. Breuner C.W., Orchinik M. Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain. J. Neuroendocrinol. 2001, 13:412-420.
8. Breuner C.W., Greenberg A.L., Wingfield J.C. Noninvasive corticosterone treatment rapidly increases activity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii). Gen. Comp. Endocrinol. 1998, 111:386-394.
9. Carrhager J.F., Rees C.M. Primary and secondary stress responses in golden perch. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 1993, 107:49-56.
10. Charlier T.D., Underhill C., Hammond G.L., Soma K.K. Effects of aggressive encounters on plasma corticosteroid-binding globulin and its ligands in white-crowned sparrows. Horm. Behav. 2009, 56:339-347.
11. Cohen A., Klasing K., Ricklefs R. Measuring circulating antioxidants in wild birds. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007, 147:110-121.
12. Cohen A.A., Hau M., Wikelski M. Stress, metabolism, and antioxidants in two wild passerine bird species. Physiol. Biochem. Zool. 2008, 81:463-472.
13. Conover W.J., Iman R.L. Rank-transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 1981, 35:124-129.
14. Corbel H., Geiger S., Groscolas R. Preparing to fledge: the adrenocortical and metabolic responses to stress in king penguin chicks. Funct. Ecol. 2010, 24:82-92.
15. Costantini D. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 2008, 11:1238-1251.
16. Curi C.M., Ribeiro E.B., Zaia C.T., Dolnikoff M.S. Glycemic response to stress stimulation by ether exposure in adrenalectomized rats. Pharmacol. Biochem. Behav. 1990, 37:399-403.
17. Cyr N.E., Wikelski M., Romero L.M. Increased energy expenditure but decreased stress responsiveness during molt. Physiol. Biochem. Zool. 2008, 81:452-462.
18. Davies S., Rodriguez N.S., Sweazea K.L., Deviche P. The effect of acute stress and long-term corticosteroid administration on plasma metabolites in an urban and desert songbird. Physiol. Biochem. Zool. 2013, 86:47-60.
19. Dawson A. Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. Gen. Comp. Endocrinol. 1983, 49:286-294.
20. Deviche P., Small T., Sharp P., Tsutsui K. Control of luteinizing hormone and testosterone secretion in a flexibly breeding male passerine, the Rufous-winged Sparrow, Aimophila carpalis. Gen. Comp. Endocrinol. 2006, 149:226-235.
21. Deviche P.J., Hurley L.L., Fokidis H.B., Lerbour B., Silverin B., Silverin B., Sabo J., Sharp P.J. Acute stress rapidly decreases plasma testosterone in a free-ranging male songbird: potential site of action and mechanism. Gen. Comp. Endocrinol. 2010, 169:82-90.
22. Deviche P., Gao S., Davies S., Sharp P.J., Dawson A. Rapid stress-induced inhibition of plasma testosterone in free-ranging male rufous-winged sparrows, Peucaea carpalis: Characterization, time course, and recovery. Gen. Comp. Endocrinol. 2012, 117:1-8.
23. Deviche P., Sharp P.J., Dawson A., Sabo J., Fokidis B., Davies S., Hurley L. Up to the challenge? Hormonal and behavioral responses of free-ranging male Cassin's sparrows, Peucaea cassinii, to conspecific song playback. Horm. Behav. 2012, 61:741-749.
24. Dlonik V.R., Gavrilov V.M. Bioenergetics of molt in the Chaffinch (Fringilla coelebs). Auk 1979, 96:253-264.
25. Dong Q., Salva A., Sottas C.M., Niu E., Holmes M., Hardy M.P. Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J. Androl. 2004, 25:973-981.
26. Fokidis H.B., Orchinik M., Deviche P. Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen. Comp. Endocrinol. 2009, 160:259-270.
27. Fokidis H.B., Hurley L., Rogowski C., Sweazea K., Deviche P. Effects of captivity and body condition on plasma corticosterone, locomotor behavior, and plasma metabolites in curve-billed thrashers. Physiol. Biochem. Zool. 2011, 84:595-606.
28. Fokidis H.B., Orchinik M., Deviche P. Context-specific territorial behavior in urban birds: no evidence for involvement of testosterone or corticosterone. Horm. Behav. 2011, 59:133-143.
29. Gill S.A., Costa L.M., Hau M. Males of a single-brooded tropical bird species do not show increases in testosterone during social challenges. Horm. Behav. 2008, 54:115-124.
30. Goutte A., Angelier F., Chastel C.C., Trouve C., Moe B., Bech C., Gabrielsen G.W., Chastel O. Stress and the timing of breeding: glucocorticoid-luteinizing hormones relationships in an arctic seabird. Gen. Comp. Endocrinol. 2010, 169:108-116.
31. Goymann W. Social modulation of androgens in male birds. Gen. Comp. Endocrinol. 2009, 163:149-157.
32. Goymann W., Landys M.M., Wingfield J.C. Distinguishing seasonal androgen responses from male-male androgen responsiveness-revisiting the Challenge Hypothesis. Horm. Behav. 2007, 51:463-476.
33. Hardy M.P., Gao H.B., Dong Q., Ge R., Wang Q., Chai W.R., Feng X., Sottas C. Stress hormone and male reproductive function. Cell Tissue Res. 2005, 322:147-153.
34. Hau M., Beebe K. Plastic endocrine regulation of year-round territorial aggression in tropical male spotted antbirds. Gen. Comp. Endocrinol. 2011, 172:305-313.
35. Herman M., Rivier C. Activation of a neural brain-testicular pathway rapidly lowers Leydig cell levels of the steroidogenic acute regulatory protein and the peripheral-type benzodiazepine receptor while increasing levels of neuronal nitric oxide synthase. Endocrinology 2006, 147:624-633.
36. Hirschenhauser K., Mostl E., Peczely P., Wallner B., Dittami J., Kotrschal K. Seasonal relationships between plasma and fecal testosterone in response to GnRH in domestic ganders. Gen. Comp. Endocrinol. 2000, 118:262-272.
37. Hirschenhauser K., Winkler H., Oliveira R.F. Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm. Behav. 2003, 43:508-519.
38. Hu G.X., Lian Q.Q., Lin H., Latif S.A., Morris D.J., Hardy M.P., Ge R.S. Rapid mechanisms of glucocorticoid signaling in the Leydig cell. Steroids 2008, 73:1018-1024.
39. James P., Rivier C., Lee S. Presence of corticotrophin-releasing factor and/or tyrosine hydroxylase in cells of a neural brain-testicular pathway that are labelled by a transganglionic tracer. J. Neuroendocrinol. 2008, 20:173-181.
40. Jawor J.M., McGlothlin J.W., Casto J.M., Greives T.J., Snajdr E.A., Bentley G.E., Ketterson E.D. Seasonal and individual variation in response to GnRH challenge in male dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 2006, 149:182-189.
41. John-Alder H.B., Cox R.M., Haenel G.J., Smith L.C. Hormones, performance and fitness: Natural history and endocrine experiments on a lizard (Sceloporus undulatus). Integr. Comp. Biol. 2009, 49:393-407.
42. Khalilieh A., McCue M.D., Pinshow B. Physiological responses to food deprivation in the house sparrow, a species not adapted to prolonged fasting. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 303:R551-R561.
43. Klukowski M. Effects of breeding season, testosterone and ACTH on the corticosterone response of free-ranging male fence lizards (Sceloporus undulatus). Gen. Comp. Endocrinol. 2011, 173:295-302.
44. Kwok A.H., Wang Y., Wang C.Y., Leung F.C. Cloning of chicken glucocorticoid receptor (GR) and characterization of its expression in pituitary and extrapituitary tissues. Poult. Sci. 2007, 86:423-430.
45. Lacombe D., Cyr A., Matton P. Plasma LH and androgen levels in the red-winged blackbird (Agelaius phoeniceus) treated with a potent GnRH analogue. Comp. Biochem. Physiol. A Comp. Physiol. 1991, 99:603-607.
46. Landys M.M., Goymann W., Raess M., Slagsvold T. Hormonal responses to male-male social challenge in the blue tit Cyanistes caeruleus: single-broodedness as an explanatory variable. Physiol. Biochem. Zool. 2007, 80:228-240.
47. Landys M.M., Goymann W., Schwabl I., Trapschuh M., Slagsvold T. Impact of season and social challenge on testosterone and corticosterone levels in a year-round territorial bird. Horm. Behav. 2010, 58:317-325.
48. Lin H., Decuypere E., Buyse J. Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 1. Chronic exposure. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2004, 139:737-744.
49. Lowther P.W., Groschupf K.D., Russell S.M. Rufous-winged Sparrow (Aimophila carpalis). The Birds of North America, No. 422 1999, The Birds of North America Inc., Philadelphia, PA. A. Poole, F. Gill (Eds.).
50. Lynn S.E., Stamplis T.B., Barrington W.T., Weida N., Hudak C.A. Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm. Behav. 2010, 58:214-222.
51. Martin L.J., Tremblay J.J. Glucocorticoids antagonize cAMP-induced Star transcription in Leydig cells through the orphan nuclear receptor NR4A1. J. Mol. Endocrinol. 2008, 41:165-175.
52. McGuire N.L., Bentley G.E. A functional neuropeptide system in vertebrate gonads: Gonadotropin-inhibitory hormone and its receptor in testes of field-caught house sparrow (Passer domesticus). Gen. Comp. Endocrinol. 2010, 166:565-572.
53. Mikics E., Kruk M.R., Haller J. Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats. Psychoneuroendocrinology 2004, 29:618-635.
54. Minick M.C. Correlation of simultaneously determined plasma insulin and glucose levels in fasting and mildly or severely stressed raptors. Comp. Biochem. Physiol. A Comp. Physiol. 1986, 83:301-305.
55. Mohammadi H., Ansari-Pirsaraei Z. Changes in some blood parameters and production performance of old laying hens due to growth hormone and testosterone injection. J. Anim. Physiol. Anim. Nutr. (Berl.) 2013, http://dx.doi.org/10.1111/jpn.12095.
56. Moore I.T., Walker B.G., Wingfield J.C. The effects of combined aromatase inhibitor and anti-androgen on male territorial aggression in a tropical population of rufous-collared sparrows, Zonotrichia capensis. Gen. Comp. Endocrinol. 2004, 135:223-229.
57. Pickering A.D., Pottinger T.G., Carragher J., Sumpter J.P. The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo trutta L. Gen. Comp. Endocrinol. 1987, 68:249-259.
58. Place N.J., Kenagy G.J. Seasonal changes in plasma testosterone and glucocorticosteroids in free-living male yellow-pine chipmunks and the response to capture and handling. J. Comp. Physiol. B 2000, 170:245-251.
59. Remage-Healey L., Romero L.M. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): glucose. Gen. Comp. Endocrinol. 2000, 119:60-68.
60. Remage-Healey L., Romero L.M. Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R994-R1003.
61. Remage-Healey L., Romero L.M. Corticosterone and insulin interact to regulate plasma glucose but not lipid concentrations in molting starlings. Gen. Comp. Endocrinol. 2002, 129:88-94.
62. Rogers C.M. An evaluation of the method of estimating body fat in birds by quantifying visible subcutaneous fat. J. Field Ornithol. 1991, 62:349-356.
63. Romero L.M. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 2002, 128:1-24.
64. Romero L.M., Remage-Healey L. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen. Comp. Endocrinol. 2000, 119:52-59.
65. Romero L.M., Ramenofsky M., Wingfield J.C. Season and migration alters the corticosterone response to capture and handling in an Arctic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelii). Comp. Biochem. Physiol. C: Comp. Pharmacol. Toxicol. Endocrinol. 1997, 116C:171-177.
66. Romero L.M., Soma K.K., Wingfield J.C. Changes in pituitary and adrenal sensitivities allow the snow bunting (Plectrophenax nivalis), an Arctic-breeding song bird, to modulate corticosterone release seasonally. J. Comp. Physiol. B 1998, 168:353-358.
67. Romero L.M, Soma K.K, Wingfield J.C. Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird. Am. J. Physiol.: Reg. Integr. Comp. Physiol. 1998, 274:R1338-R1344.
68. Romero L.M., Strochlic D., Wingfield J.C. Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2005, 142:65-73.
69. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
70. Siegel S. Nonparametric Statistics for the Behavioral Sciences 1956, McGraw-Hill, New York, 312pp.
71. Silverin B., Baillien M., Balthazart J. Territorial aggression, circulating levels of testosterone, and brain aromatase activity in free-living pied flycatchers. Horm. Behav. 2004, 45:225-234.
72. Small T.W., Sharp P.J., Deviche P. Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the Rufous-winged Sparrow, Aimophila carpalis. Horm. Behav. 2007, 51:483-495.
73. Stinefelt B., Leonard S.S., Blemings K.P., Shi X., Klandorf H. Free radical scavenging, DNA protection, and inhibition of lipid peroxidation mediated by uric acid. Ann. Clin. Lab. Sci. 2005, 35:37-45.
74. Strochlic D.E., Romero L.M. The effects of chronic psychological and physical stress on feather replacement in European starlings (Sturnus vulgaris). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2008, 149:68-79.
75. Summers C.H., Winberg S. Interactions between the neural regulation of stress and aggression. J. Exp. Biol. 2006, 209:4581-4589.
76. Tsahar E., Arad Z., Izhaki I., Guglielmo C.G. The relationship between uric acid and its oxidative product allantoin: a potential indicator for the evaluation of oxidative stress in birds. J. Comp. Physiol. B 2006, 176:653-661.
77. Van Duyse D.E., Pinxten R., Eens M. Seasonal fluctuations in plasma testosterone levels and diurnal song activity in free-living male great tits. Gen. Comp. Endocrinol. 2003, 134:1-9.
78. Van Duyse E., Pinxten R., Darras V.M., Arckens L., Eens M. Opposite changes in plasma testosterone and corticosterone levels following a simulated territorial challenge in great tits. Behaviour 2004, 141:451-467.
79. Wakita T., Ohmori Y., Watanabe T., Fukuta K. Location of sympathetic postganglionic and sensory neurons innervating the testis in the male chicken. Anat. Histol. Embryol. 1999, 28:299-302.
80. Wikelski M., Hau M., Wingfield J. Social instability increases plasma testosterone in a year-round territorial neotropical bird. Proc. R. Soc. London B 1999, 22:551-556.
81. Wingfield J.C. Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna. Horm. Behav. 1994, 28:1-15.
82. Wingfield J.C., Farner D.S. The endocrinology of a natural breeding population of the White-crowned Sparrow (Zonotrichia leucophrys pugetensis). Physiol. Zool. 1978, 51:188-205.
83. Wingfield J.C., Kitaysky A.S. Endocrine responses to unpredictable environmental events: stress or anti-stress hormones?. Integr. Comp. Biol. 2002, 42:600-609.
84. Wingfield J.C., Wada M. Changes in plasma levels of testosterone during male-male interactions in the Song Sparrow, Melospiza melodia: time course and specificity of response. J. Comp. Phyiol. A: Sensory, Neural Behav. Physiol. 1989, 166:189-194.
85. Wingfield J.C., Smith M.J., Farner D.S. Endocrine responses of White-crowned Sparrows to environmental stress. Condor 1982, 84:399-409.
86. Wingfield J., Ball G.F., Dufty A.M., Hegner R.E., Ramenofsky M. Testosterone and aggression in birds. Am. Sci. 1987, 75:602-608.
87. Wingfield J.C., Hegner R.E., Dufty A.M., Ball G.F. The "Challenge Hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 1990, 136:829-846.
88. Wingfield J., Maney D., Breuner C., Jacobs J.D., Lynn S., Ramenofsky M., Richardson R.D. Ecological basis of hormone-behavior interactions: The "emergency life history stage". Integr. Comp. Biol. 1998, 38:191-206.
89. Woodley S.K., Lacy E.L. An acute stressor alters steroid hormone levels and activity but not sexual behavior in male and female Ocoee salamanders (Desmognathus ocoee). Horm. Behav. 2010, 58:427-432.