Carotenoid supplementation and GnRH challenges influence female endocrine physiology, immune function, and egg-yolk characteristics in Japanese quail (Coturnix japonica)

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 182, Issue 5, 2012, Pages 687-702

  Peluc, Susana I ^a,c   Reed, Wendy L ^a   McGraw, Kevin J ^b   Gibbs, Penelope ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c CENTRO DE ZOOLOGÍA APLICADA   (Argentina)

Author keywords

Acquired immunity; Innate immunity; Maternal effects; PHA; Testosterone; Vitamin E; Yolk carotenoids; Yolk steroids

Indexed keywords

CAROTENOID; DIAGNOSTIC AGENT; GONADORELIN; TESTOSTERONE; XANTHOPHYLL; ZEAXANTHIN;

ANIMAL; ARTICLE; BLOOD; CHEMISTRY; COTURNIX; DIET SUPPLEMENTATION; DRUG EFFECT; EGG YOLK; FEMALE; IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; PHYSIOLOGY;

ANIMALS; CAROTENOIDS; COTURNIX; DIETARY SUPPLEMENTS; EGG YOLK; FEMALE; GONADOTROPIN-RELEASING HORMONE; IMMUNITY; IMMUNOSUPPRESSION; LUTEIN; TESTOSTERONE; XANTHOPHYLLS;

EID: 84862668291     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-011-0638-3     Document Type: Article

References (133)

1. Adamo SA (2004) How should behavioural ecologists interpret measurements of immunity? Anim Behav 68: 1443-1449.
2. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Ser B Biol Sci 274: 819-825.
3. Bertin A, Richard-Yris MA, Houdelier C, Lumineau S, Mostl E, Kuchar A, Hirschenhauser K, Kotrschal K (2008) Habituation to humans affects yolk steroid levels and offspring phenotype in quail. Horm Behav 54: 396-402.
4. Biard C, Surai PF, Møller AP (2007) An analysis of pre-and post-hatching maternal effects mediated by carotenoids in the blue tit. J Evol Biol 20: 326-339.
5. Blas J, Pérez-Rodriguez L, Bortolotti GR, Viñuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc Natl Acad Sci USA 103: 18633-18637.
6. Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond Ser B Biol Sci 269: 29-36.
7. Blount JD, Houston DC, Moller AP, Wright J (2003a) Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds. Oikos 102: 340-350.
8. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003b) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300: 125-127.
9. Blount JD, Houston DC, Surai PF, Møller AP (2004) Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proc R Soc Lond Ser B Biol Sci 271: S79-S81.
10. Boonstra TA, Clark ME, Reed WL (2009) Maternal resource variation across the laying sequence in Canada geese Branta canadensis maxima. J Avian Biol 40: 520-528.
11. Bortolotti GR, Negro JJ, Surai PF, Prieto P (2003) Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiol Biochem Zool 76: 367-374.
12. Boughton RK, Bridge ES, Schoech SJ (2007) Energetic trade-offs between immunity and reproduction in male Japanese quail (Coturnix coturnix). J Exp Zool Part A 307A: 479-487.
13. Caprio E, Ellena I, Rolando A (2009) Native oak retention as a key factor for the conservation of winter bird diversity in managed deciduous forests in northern Italy. Landsc Ecol 24: 65-76.
14. Casto JM, Nolan V, Ketterson ED (2001) Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157: 408-420.
15. Cawthorn JM, Morris DL, Ketterson ED, Nolan V (1998) Influence of experimentally elevated testosterone on nest defence in dark-eyed juncos. Anim Behav 56: 617-621.
16. Clotfelter ED, O'Neal DM, Gaudioso JM, Casto JM, Parker-Renga IM, Snajdr EA, Duffy DL, Nolan V, Ketterson ED (2004) Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Horm Behav 46: 171-178.
17. Cucco M, Guasco B, Malacarne G, Ottonelli R, Tanvez A (2008) Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen Comp Endocrinol 156: 418-425.
18. Daisley JN, Bromundt V, Mostl E, Kotrschal K (2005) Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. Horm Behav 47: 185-194.
19. Deviche P, Cortez L (2005) Androgen control of immunocompetence in the male house finch, Carpodacus mexicanus Muller. J Exp Biol 208: 1287-1295.
20. Duffy DL, Bentley GE, Drazen DL, Ball GF (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 11: 654-662.
21. Eising CM, Eikenaar C, Schwbl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond Ser B Biol Sci 268: 839-846.
22. Eising CM, Muller W, Groothuis TGG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2: 20-22.
23. Elekonich MM, Wingfield JC (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Ethology 106: 493-510.
24. El-Lethey H, Huber-Eicher B, Jungi TW (2003) Exploration of stress-induced immunosuppression in chickens reveals both stress-resistant and stress-susceptible antigen responses. Vet Immunol Immunopathol 95: 91-101.
25. Ewen JG, Thorogood R, Brekke P, Cassey P, Karadas F, Armstrong DP (2009) Maternally invested carotenoids compensate costly ectoparasitism in the hihi. Proc Natl Acad Sci USA 106: 12798-12802.
26. Gil D (2003) Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50: 281-294.
27. Gil D (2008) Hormones in avian eggs: physiology, ecology and behavior. Advances in the study of behavior. Elsevier, San Diego, pp 337-398.
28. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286: 126-128.
29. Gil D, Biard C, Lacroix A, Spottiswoode CN, Saino N, Puerta M, Møller AP (2007) Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am Nat 169: 802-819.
30. Goodwin TW (1986) Metabolism, nutrition, and function of carotenoids. Annu Rev Nutr 6: 273-297.
31. Goymann W, Wingfield JC (2004) Competing females and caring males. Sex steroids in African black coucals, Centropus grillii. Anim Behav 68: 733-740.
32. Groothuis TGG, von Engelhardt N (2005) Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation. Ann NY Acad Sci 1046: 168-180.
33. Groothuis TGG, Muller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29: 329-352.
34. Groothuis TGG, Eising CM, Blount JD, Surai P, Apanius V, Dijkstra C, Muller W (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J Evol Biol 19: 1304-1313.
35. Hackl R, Bromundt V, Daisley J, Kotrschal K, Mostl E (2003) Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J Comp Physiol B Biochem Syst Environ Physiol 173: 327-331.
36. Haq AU, Bailey CA, Chinnah A (1996) Effect of beta-carotene, canthaxanthin, lutein, and vitamin E on neonatal immunity of chicks when supplemented in the broiler breeder diets. Poult Sci 75: 1092-1097.
37. Hasselquist D, Marsh JA, Sherman PW, Wingfield JC (1999) Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45: 167-175.
38. Hau M, Wikelski M, Soma KK, Wingfield JC (2000) Testosterone and year-round territorial aggression in a tropical bird. Gen Comp Endocrinol 117: 20-33.
39. Hegner RE, Wingfield JC (1987) Social-status and circulating levels of hormones in flocks of house sparrows, Passer domesticus. Ethology 76: 1-14.
40. Hirschenhauser K, Mostl E, Peczely P, Wallner B, Dittami J, Kotrschal K (2000) Seasonal relationships between plasma and fecal testosterone in response to GnRH in domestic ganders. Gen Comp Endocrinol 118: 262-272.
41. Huss D, Poynter G, Lansford R (2008) Japanese quail (Coturnix japonica) as a laboratory animal model. Lab Anim 37: 513-519.
42. Jawor JM, Young R, Ketterson ED (2006) Females competing to reproduce: dominance matters but testosterone may not. Horm Behav 49: 362-368.
43. Jawor JM, McGlothlin JW, Casto JM, Greives TJ, Snajdr EA, Bentley GE, Ketterson ED (2007) Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects. Funct Ecol 21: 767-775.
44. Jayasooriya AP, Weisinger RS, Weisinger HS, Mathai ML, Sinclair AJ (2002) Attraction to orange: sexiness, not gluttony. Science 296: 847-848.
45. Johnson AL (2000) Reproduction in the female. In: Whittow GC (ed) Sturkie's avian physiology. Academic Press, San Diego, pp 569-596.
46. Ketterson ED, Nolan V (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154: S4-S25.
47. Ketterson ED, Nolan V, Wolf L, Ziegenfus C, Dufty AM, Ball GF, Johnsen TS (1991) Testosterone and avian life histories-the effect of experimentally elevated testosterone on corticosterone and body-mass in dark-eyed juncos. Horm Behav 25: 489-503.
48. Ketterson ED, Nolan V, Sandell M (2005) Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both? Am Nat 166: S85-S98.
49. Ketterson ED, Atwell JW, McGlothlin JW (2009) Phenotypic integration and independence: hormones, performance, and response to environmental change. Integr Comp Biol 49: 365-379.
50. Kingma SA, Komdeur J, Vedder O, von Engelhardt N, Korsten P, Groothuis TGG (2009) Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition. Behav Ecol 20: 172-179.
51. Klukowski LA, Cawthorn JM, Ketterson ED, Nolan V (1997) Effects of experimentally elevated testosterone on plasma corticosterone and corticosteroid-binding globulin in dark-eyed juncos (Junco hyemalis). Gen Comp Endocrinol 108: 141-151.
52. Koutsos EA, Lopez JCG, Klasing KC (2006) Carotenoids from in ovo or dietary sources blunt systemic indices of the inflammatory response in growing chicks (Gallus gallus domesticus). J Nutr 136: 1027-1031.
53. Krinsky NI (2001) Carotenoids as antioxidants. Nutrition 17: 815-817.
54. Lacombe D, Cyr A, Matton P (1991) Plasma-Lh and androgen levels in the red-winged blackbird (Agelaiusphoeniceus) treated with a potent GnRH analog. Comp Biochem Physiol A Physiol 99: 603-607.
55. Langmore NE, Cockrem JF, Candy EJ (2002) Competition for male reproductive investment elevates testosterone levels in female dunnocks, Prunella modularis. Proc R Soc Lond Ser B Biol Sci 269: 2473-2478.
56. Lees AC, Peres CA (2008) Avian life-history determinants of local extinction risk in a hyper-fragmented neotropical forest landscape. Anim Conserv 11: 128-137.
57. Leitner G, Landsman T, Blum O, Zaltsmann N, Heller ED (1996) Effects of gonadal steroids and their antagonists on the humoral immune response of immune-selected broiler chicks. Poult Sci 75: 1373-1382.
58. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities-a common mistake. Auk 104: 116-121.
59. Lindström KM, Krakower D, Lundström JO, Silverin B (2001) The effects of testosterone on a viral infection in greenfinches (Carduelis chloris): an experimental test of the immunocompetence-handicap hypothesis. Proc R Soc Lond Ser B Biol Sci 268: 207-211.
60. Lochmiller RL (1995) Testing the immunocompetence handicap theory. Trends Ecol Evol 10: 372-373.
61. Lopez-Rull I, Gil D (2009) Elevated testosterone levels affect female breeding success and yolk androgen deposition in a passerine bird. Behav Processes 82: 312-318.
62. Matson KD, Tieleman BI, Klasing KC (2006) Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiol Biochem Zool 79: 556-564.
63. Mazuc J, Bonneaud C, Chastel O, Sorci G (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 6: 1084-1090.
64. McCay PB (1985) Vitamin-E-interactions with free-radicals and ascorbate. Annu Rev Nutr 5: 323-340.
65. McGraw KJ (2006a) Dietary carotenoids mediate a trade-off between egg quantity and quality in Japanese quail. Ethol Ecol Evol 18: 247-256.
66. McGraw KJ (2006b) Sex steroid dependence of carotenoid-based coloration in female zebra finches. Physiol Behav 88: 347-352.
67. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162: 704-712.
68. McGraw KJ, Ardia DR (2005) Sex differences in carotenoid status and immune performance in zebra finches. Evol Ecol Res 7: 251-262.
69. McGraw KJ, Ardia DR (2007) Do carotenoids buffer testosterone-induced immunosuppression? An experimental test in a colourful songbird. Biol Lett 3: 375-378.
70. McGraw KJ, Klasing KC (2006) Carotenoids, immunity, and integumentary coloration in red junglefowl (Gallus gallus). Auk 123: 1161-1171.
71. McGraw KJ, Parker RS (2006) A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird. Physiol Behav 87: 103-108.
72. McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92: 375-380.
73. McGraw KJ, Correa SM, Adkins-Regan E (2006a) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60: 117-122.
74. McGraw KJ, Crino OL, Medina-Jerez W, Nolan PM (2006b) Effect of dietary carotenoid supplementation on food intake and immune function in a songbird with no carotenoid coloration. Ethology 112: 1209-1216.
75. McGraw KJ, Nolan PM, Crino OL (2011) Carotenoids bolster immunity during moult in a wild songbird with sexually selected plumage coloration. Biol J Linn Soc 102: 560-572.
76. Mendes L, Piersma T, Hasselquist D, Matson KD, Ricklefs RE (2006) Variation in the innate and acquired arms of the immune system among five shorebird species. J Exp Biol 209: 284-291.
77. Moore IT, Perfito N, Wada H, Sperry TS, Wingfield JC (2002) Latitudinal variation in plasma testosterone levels in birds of the genus Zonotrichia. Gen Comp Endocrinol 129: 13-19.
78. Navara KJ, Badyaev AV, Mendonca MT, Hill GE (2006a) Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiol Biochem Zool 79: 1098-1105.
79. Navara KJ, Siefferman LM, Hill GE, Mendonca MT (2006b) Yolk androgens vary inversely to maternal androgens in eastern bluebirds: an experimental study. Funct Ecol 20: 449-456.
80. Newbrey JL, Reed WL (2009) Growth of yellow-headed blackbird Xanthocephalus xanthocephalus nestlings in relation to maternal body condition, egg mass, and yolk carotenoids concentrations. J Avian Biol 40: 419-429.
81. O'Neal DM, Reichard DG, Pavilis K, Ketterson ED (2008) Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the dark-eyed junco (Junco hyemalis). Horm Behav 54: 571-578.
82. Okuliarova M, Skrobanek P, Zeman M (2007) Effect of increasing yolk testosterone levels on early behaviour in Japanese quail hatchlings. Acta Vet Brno 76: 325-331.
83. Ottinger MA, Brinkley HJ (1979) Testosterone and sex related physical characteristics during the maturation of the male Japanese quail (Coturnix-coturnix-japonica). Biol Reprod 20: 905-909.
84. Owen-Ashley NT, Hasselquist D, Wingfield JC (2004) Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 164: 490-505.
85. Peters A (2000) Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc R Soc Lond Ser B Biol Sci 267: 883-889.
86. Peters A (2007) Testosterone and carotenoids: an integrated view of trade-offs between immunity and sexual signalling. Bioessays 29: 427-430.
87. Pilz KM, Smith HG (2004) Egg yolk androgen levels increase with breeding density in the European Starling, Sturnus vulgaris. Funct Ecol 18: 58-66.
88. Pilz KM, Smith HG, Sandell MI, Schwabl H (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim Behav 65: 841-850.
89. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68: 227-239.
90. Roberts ML, Buchanan KL, Evans MR, Marin RH, Satterlee DG (2009) The effects of testosterone on immune function in quail selected for divergent plasma corticosterone response. J Exp Biol 212: 3125-3131.
91. Robinson JE, Follett BK (1982) Photoperiodism in Japanese quail-the termination of seasonal breeding by photorefractoriness. Proc R Soc Lond Ser B Biol Sci 215: 95-116.
92. Ros AFH, Groothuis TGG, Apanius V (1997) The relation among gonadal steroids, immunocompetence, body mass, and behavior in young black-headed gulls (Larus ridibundus). Am Nat 150: 201-219.
93. Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12: 381-385.
94. Rutkowska J, Cichon M, Puerta M, Gil D (2005) Negative effects of elevated testosterone on female fecundity in zebra finches. Horm Behav 47: 585-591.
95. Rutkowska J, Wilk T, Cichon M (2007) Androgen-dependent maternal effects on offspring fitness in zebra finches. Behav Ecol Sociobiol 61: 1211-1217.
96. Safran RJ, Pilz KM, McGraw KJ, Correa SM, Schwabl H (2008) Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behav Ecol Sociobiol 62: 427-438.
97. Safran RJ, McGraw KJ, Pilz KM, Correa SM (2010) Egg-yolk androgen and carotenoid deposition as a function of maternal social environment in barn swallows Hirundo rustica. J Avian Biol 41: 470-478.
98. Saino N, Møller AP, Bolzern AM (1995) Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behav Ecol 6: 397-404.
99. Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond Ser B Biol Sci 270: 2485-2489.
100. SAS Institute (2006) JMP. Version 5. 0. 1. 2. SAS Institute, Cary, North Carolina.
101. Schoech SJ, Ketterson ED, Nolan V (1999) Exogenous testosterone and the adrenocortical response in dark-eyed juncos. Auk 116: 64-72.
102. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90: 11446-11450.
103. Schwabl H (1996) Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276: 157-163.
104. Schwabl H (1997) The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84: 406-408.
105. Sepp T, Karu U, Sild E, Manniste M, Hõrak P (2011) Effects of carotenoids, immune activation and immune suppression on the intensity of chronic coccidiosis in greenfinches. Exp Parasitol 127: 651-657.
106. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11: 317-321.
107. Smith LC, Raouf SA, Brown MB, Wingfield JC, Brown CR (2005) Testosterone and group size in cliff swallows: testing the "challenge hypothesis" in a colonial bird. Horm Behav 47: 76-82.
108. Smits JE, Williams TD (1999) Validation of immunotoxicology techniques in passerine chicks exposed to oil sands tailings water. Ecotoxicol Environ Saf 44: 105-112.
109. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13: 567-572.
110. Soma KK, Wingfield JC (2001) Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen Comp Endocrinol 123: 144-155.
111. Staub NL, DeBeer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108: 1-24.
112. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3: 259-268.
113. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56: 491-497.
114. Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9: 645-651.
115. Surai PF, Noble RC, Speake BK (1999a) Relationship between vitamin E content and susceptibility to lipid peroxidation in tissues of the newly hatched chick. Br Poult Sci 40: 406-410.
116. Surai PF, Speake BK, Noble RC, Sparks NHC (1999b) Tissue-specific antioxidant profiles and susceptibility to lipid peroxidation of the newly hatched chick. Biol Trace Elem Res 68: 63-78.
117. Surai PF, Speake BK, Decrock F, Groscolas R (2001a) Transfer of vitamins E and A from yolk to embryo during development of the king penguin (Aptenodytes patagonicus). Physiol Biochem Zool 74: 928-936.
118. Surai PF, Speake BK, Sparks NHC (2001b) Carotenoids in avian nutrition and embryonic development. 2. Antioxidant properties and discrimination in embryonic tissues. J Poult Sci 38: 117-145.
119. Surai PF, Speake BK, Wood NAR, Blount JD, Bortolotti GR, Sparks NHC (2001c) Carotenoid discrimination by the avian embryo: a lesson from wild birds. Comp Biochem Physiol B Biochem Mol Biol 128: 743-750.
120. Tanvez A, Amy M, Chastel O, Leboucher G (2009) Maternal effects and beta-carotene assimilation in canary chicks. Physiol Behav 96: 389-393.
121. Tobler M, Hasselquist D, Smith HG, Sandell MI (2010) Short-and long-term consequences of prenatal testosterone for immune function: an experimental study in the zebra finch. Behav Ecol Sociobiol 64: 717-727.
122. Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H (2005) Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol 74: 675-682.
123. Verboven N, Evans NP, D'Alba L, Nager RG, Blount JD, Surai PF, Monaghan P (2005) Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav Ecol Sociobiol 57: 357-365.
124. Wayland M, Gilchrist HG, Marchant T, Keating J, Smits JE (2002) Immune function, stress response, and body condition in arctic-breeding common eiders in relation to cadmium, mercury, and selenium concentrations. Environ Res 90: 47-60.
125. Whittingham LA, Schwabl H (2002) Maternal testosterone in tree swallow eggs varies with female aggression. Anim Behav 63: 63-67.
126. Wingfield JC, Farner DS (1979) Some endocrine correlates of renesting after loss of clutch or brood in the white-crowned sparrow, Zonotrichia-leucophrys-gambelii. Gen Comp Endocrinol 38: 322-331.
127. Wingfield JC, Matt KS, Farner DS (1984) Physiologic properties of steroid hormone-binding proteins in avian blood. Gen Comp Endocrinol 53: 281-292.
128. Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The challenge hypothesis-theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136: 829-846.
129. Wooley RE, Nolan LK, Brown J, Gibbs PS, Giddings CW, Turner KS (1993) Association of K-1 capsule, smooth lipopolysaccharides, traT gene, and colicin V production with complement resistance and virulence of avian Escherichia coli. Avian Dis 37: 1092-1096.
130. Young AJ, Lowe GM (2001) Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 385: 20-27.
131. Zuk M, Johnsen TS (1998) Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc R Soc Lond Ser B Biol Sci 265: 1631-1635.
132. Zuk M, Johnsen TS, Maclarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond Ser B Biol Sci 260: 205-210.
133. Zysling DA, GreiveS TJ, Breuner CW, Casto JM, Dernas GE, Ketterson ED (2006) Behavioral and physiological responses to experimentally elevated testosterone in female dark-eyed juncos (Junco hyemalis carolinensis). Horm Behav 50: 200-207.