Carotenoid-dependent Signals: Indicators of Foraging Efficiency, Immunocompetence or Detoxification Ability?

Avian and Poultry Biology Reviews

Volumn 11, Issue 3, 2000, Pages 137-159

  Moller A P ^a   Biard, C ^a   Blount, J D ^b   Houston, D C ^b   Ninni, P ^a   Saino, N ^c   Surai, P F ^d  

^a UPMC University Paris 06   (France)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d SCOTTISH AGRICULTURAL COLLEGE   (United Kingdom)

Author keywords

Detoxification; Immune function; Limitation of carotenoids; Offspring signals; Parasitism; Sexual selection

Indexed keywords

EID: 0348097521     PISSN: 14702061     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (241)

1. Allard, J.P., Royall, D., Kurian, R., Muggli, R. and Jeejeebhoy, K.N. 1994. Effects of beta-carotene supplementation on lipid peroxidation in humans. Am. J. Clin. Nutr., 59, 884-890.
2. Allen, P.C. 1997. Production of free radical species during Eimeria maxima infections in chickens. Poultry Sci., 76, 814-821
3. Ames, B.N. 1983. Dietary carcinogens and anticarcinogens: Oxygen radicals and degenerative diseases. Science, 221, 1256-1264.
4. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton.
5. Bakker, T.C.M. and Sevenster, P. 1983. Determinants of dominance in male sticklebacks (Gasterosteus aculeatus L.). Behaviour, 86, 55-71.
6. Bast, A., Haenen, G.R., van den Berg, R. and van den Berg, H. 1998. Antioxidant effects of carotenoids. Int. J. vitam. Nutr. Res., 68, 399-403.
7. BenAmotz, A., Rachmilevich, B., Greenberg, S., Sela, M. and Weshler, Z. 1996. Natural beta-carotene and whole body irradiation in rats. Rad. Environm, Biophys., 35, 285-288.
8. Bendich, A. 1989. Carotenoids and the Immune Response. J. Nutr., 119, 112-115.
9. Bennett, A.T.D., Cuthill, I.C., Partridge, J.C. and Maier, E.J. 1996. Ultraviolet vision and mate choice in zebra finches. Nature, 380, 433-435.
10. Bertram, J.S. 1999. Carotenoids and gene regulation. Nutr. Rev., 57, 182-191.
11. Blakely, S.R., Slaughter, L., Adkins, J. and Knight, E.V. 1988. Effects of beta-carotene and retinyl palmitate on corn oil-induced superoxide dismutase and catalase in rats. J. Nutr., 118, 152-158.
12. Bletner, J.K., Jr., Mitchell, Jr., R.P. and Tugwell, R.L. 1966. The Effect of Eimeria maxima on Broiler Pigmentation. Poultry Sci., 45, 689-694.
13. Blount, J.D., Houston, D.C. and Møller, A.P. 2000. Why egg yolk is yellow. Trends Ecol. Evol., 15, 47-49.
14. Böhm, F., Edge, R., Land, E.J., McGarvey, D.J. and Truscott, T.G. 1997. Carotenoids enhance vitamin E antioxidant efficiency. J. Am. Chem. Soc., 119, 621-622.
15. Bohm, F., Edge, R., McGarvey, D.J. and Truscott, T.G. 1998. Beta-carotene with vitamins E and C offers synergistic cell protection against NOx. FEBS Lett., 436, 387-389.
16. Bortolotti, G.R., Negro, J.J., Tella, J.L., Marchant, T.A. and Bird, D.M. 1996. Sexual dichromatism in birds independent of diet, parasites and androgens. Proc. R. Soc. Lond., B 263, 1171-1176.
17. Brodsky, L. 1988. Ornament size influences mating success in male rock ptarmigan. Anim. Behav., 36, 662-667.
18. Bronseth, T. and Folstad, I. 1997. The effect of parasites on courtship dance in three-spined sticklebacks: more than meets the eye? Can. J. Zool., 75, 589-594.
19. Brush, A. 1981. Carotenoids in wild and captive birds. In Carotenoids as colorants and vitamin A precursors, ed Bauernfeind, J.C. Academic Press, New York, pp. 539-562.
20. Brush, A.H. and Power, D.M. 1976. House finch pigmentation: carotenoid metabolism and the effect of diet. Auk, 93, 725-739.
21. Buchholz, R. 1995. Female choice, parasite load and male ornamentation in wild turkeys. Anim. Behav., 50, 929-943.
22. Burley, N. 1986a. Comparison of the band-colour preferences of two species of estrildid finches. Anim. Behav., 34, 1732-1741.
23. Burley, N. 1986b. Sexual selection for aesthetic traits in species with biparental care. Am. Nat., 127, 415-445.
24. Burley, N. 1988. Wild zebra finches have band-colour preferences. Anim. Behav., 36, 1235-1237.
25. Burley, N. and Coopersmith, C.B. 1987. Bill colour preferences of zebra finches. Ethology, 76, 133-151.
26. Burley, N.T., Enstrom, D.A. and Chitwood, L. 1994. Extra-pair relations in zebra finches: Differential male success results from female tactics. Anim. Behav., 48, 1031-1041.
27. Burley, N.T., Parker, P.G. and Lundy, K. 1996. Sexual selection and extrapair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia guttata). Behav. Ecol., 7, 218-226.
28. Burley, N.T. and Price, D.K. 1991. Extra-pair copulation and attractiveness in zebra finches. Acta Congr. Int. Orn., 20, 1367-1372.
29. Burley, N., Tidemann, S.C. and Halupka, K. 1991. Bill colour and parasite levels of zebra finches. In Bird-parasite interactions: ecology, evolution and behaviour, eds Loye, J.E. and Zuk, M. Oxford University Press, Oxford, pp. 359-375.
30. Camplani, A., Saino, N. and Møller, A.P. 1999. Carotenoids, sexual signals and immune function in barn swallows from Chernobyl. Proc. R. Soc. Lond., B 266, 1111-1116.
31. Carbonneau, M.A., Melin, A.M., Perromat, A. and Clerc, M. 1989. The action of free radicals on Deinococcus radiodurans carotenoids. Arch. Biochem. Biophys., 275, 244-251
32. Carpenter, K.L., van der Veen, C., Hird, R., Dennis, I.F., Ding, T. and Mitchinson, M.J. 1997. The carotenoids beta-carotene, canthaxanthin and zeaxanthin inhibit macrophage-mediated LDL oxidation. FEBS Lett., 401, 262-266.
33. Chapple, I.L. 1997. Reactive oxygen species and antioxidants in inflammatory diseases. J. Clin. Periodontol., 24, 287-296.
34. Chew, B.P. 1993. Role of carotenoids in the immune response. J. Dairy Sci., 76, 2804-2811.
35. Chew, B.P. 1996. Importance of antioxidant vitamins in immunity and health in animals. Anim. Feed Sci. Technol., 59, 103-114.
36. Chew, B.P., Park, J.S., Wong, M.W. and Wong T.S. 1999. A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res., 19, 1849-1853.
37. Chew, B.P., Wong, M.W. and Wong, T.S. 1996. Effects of lutein from marigold extract on immunity and growth of mammary tumors in mice. Anticancer Res., 16, 3689-3694.
38. Christiansen, R., Glette, J., Lie, O., Torrissen, O.J. and Waagbo, R. 1995. Antioxidant status and immunity in Atlantic salmon, Salmo salar L., fed semi-purified diets with and without astaxanthin supplementation. J. Fish Dis., 18, 317-328.
39. Collias, E.C., Collias, N.E., Jacobs, C.H., McAlary, F. and Fujimoto, J.T. 1979. Experimental evidence for facilitation of pair formation by bright color in weaverbirds. Condor, 81, 91-93.
40. Collins, S.A., Hubbard, C. and Houtman, A.M. 1994. Female mate choice in the zebra finch - the effect of male beak colour and male song. Behav. Ecol. Sociobiol., 35, 21-25.
41. Damron, B.L., Goodson, S.R., Harms, R.H., Janly, D.M. and Wilson, H.R. 1984. β-carotene supplementation of laying hen diets. Br. Poult. Sci., 25, 349-352.
42. De Flora, S., Bagnasco, M. and Vainio, H. 1999. Modulation of genotoxic and related effects by carotenoids and vitamin A in experimental models: mechanistic issues. Mutagenesis, 14, 153-172.
43. De Mejia, E.G., RamosGomez, M. and LoarcaPina, G. 1997. Antimutagenic activity of natural xanthophylls against aflatoxin B-1 in Salmonella typhimurium. Environ. Molecular Mutagen, 30, 346-353.
44. De Mejia, E.G., Loarca-Pina, G., Ramos-Gomez, M. 1997a. Antimutagenicity of xanthophylls present in Aztec Marigold (Tagetes erecta) against 1-nitropyrene. Mutat. Res., 389, 219-226.
45. Dixon, Z.R., Burri, B.J., Clifford, A., Frankel, E.N., Schneeman, B.O., Parks, E., Keim, N.L., Barbieri, T., Wu, M.M., Fong, A.K., Kretsch, M.J., Sowell, A.L. and Erdman, J.W. 1994. Effects of a carotene-deficient diet on measures of oxidative susceptibility and superoxide dismutase activity in adult women. Free Rad. Biol. Med., 17, 537-544.
46. Dufva, R. and Allander, K. 1995. Intraspecific variation in plumage coloration reflects immune response in great tit (Parus major) males. Funct. Ecol., 9, 785-789.
47. Dugas, T.R., Morel, D.W. and Harrison, E.H. 1998. Impact of LDL carotenoid and α-tocopherol content on LDL oxidation by endothelial cells in culture. J. Lipid. Res., 39, 999-1007.
48. Dugas, T.R., Morel, D.W. and Harrison, E.H. 1999. Dietary supplementation with beta-carotene, but not with lycopene, inhibits endothelial cell-mediated oxidation of low-density lipoprotein. Free Radic. Biol. Med., 26, 1238-1244.
49. Edge, R., McGarvey, D.J. and Truscott, T.G. 1997. The carotenoids as antioxidants - a review. J. Photochem. Photobiol., 41B, 189-200.
50. Eeva, T., Lehikoinen, E. and Rönkä, M. 1998. Air pollution fades the plumage of the Great Tit. Funct. Ecol., 12, 607-612.
51. Endler, J.A. 1980. Natural selection on color patterns in Poecilia reticulata. Evolution, 34, 76-91.
52. Endler, J.A. 1983. Natural and sexual selection on colour pattern in poeciliid fishes. Environ. Biol. Fishes, 9, 173-190.
53. Figuerola, J. and Gutiérrez, R. 1998. Sexual differences in levels of blood carotenoids in cirl buntings Emberiza cirlus. Ardea, 86, 245-248.
54. Figuerola, J., Muñoz, E., Gutiérrez, R. and Ferrer, D. 1999. Blood parasites, leucocytes and plumage brightness in the Cirl Bunting, Emberiza cirlus. Funct. Ecol., 13, 594-601.
55. Fitzgerald, G.J., Fournier, M. and Morrissette, J. 1993. Sexual selection in an anadromus population of threespine sticklebacks - no role for parasites. Evol. Ecol., 8, 348-356.
56. Fletcher, J. 1992. Methodology for achieving pigment specifications. Poultry Sci., 71, 733-743.
57. Folstad, I., Hope, A.M., Karter, A. and Skørping, A. 1994. Sexually selected colour in male sticklebacks: a signal of both parasite exposure and parasite resistance. Oikos, 69, 511-515.
58. Forssberg, A., Lingen, C., Ernster, L. and Lindberg, O. 1959. Modification of the x-irradiation syndrome by lycopene. Exp. Cell. Res., 16, 7-14.
59. Fox, D.L. 1979. Biochromy. University of California Press, Berkeley.
60. Franke, A.A., Harwood, P.J., Shimamoto, T., Lumeng, S., Zhang, L.X., Bertram, J.S., Wilkens, L.R., Le Marchand, L. and Cooney, R.V. 1994. Effects of micronutrients and antioxidants on lipid peroxidation in human plasma and in cell culture. Cancer Lett., 79, 17-26.
61. Gille, G. and Sigler, K. 1995. Oxidative stress and living cells. Folia Microbiol, (Praha) 40, 131-152.
62. Godfray, H.C.J. 1991 Signalling of need by offspring to their parents. Nature, 352, 328-330.
63. Godfray, H.C.J. 1995 Signalling of need between parents and young, parent-offspring conflict and sibling rivalry. Am. Nat., 142, 1-24.
64. Goodwin, T.W. 1984. The biochemistry of the carotenoids. Vol. II. Animals. Chapman and Hall, London.
65. Götmark, F. and Ahlstrom, M. 1997. Parental preference for red mouth of chicks in a songbird. Proc. R. Soc. Lond. B, 264, 959-962.
66. Götmark, F. and Olsson, J. 1997. Artificial colour mutation: do red-painted great tits experience increased or decreased predation? Anim. Behav., 53, 83-91.
67. Gottlieb, K., Zarling, E.J., Mobarhan, S., Bowen, P. and Sugerman, S. 1993. Beta-carotene decreases markers of lipid peroxidation in healthy volunteers. Nutr. Cancer, 19, 207-212.
68. Gradelet, S., Astorg, P., Le Bon, A.M., Berges, R. and Suschetet, M. 1997. Modulation of aflatoxin B1 carcinogenicity, genotoxicity and metabolism in rat liver by dietary carotenoids: evidence for a protective effect of CYP1A inducers. Cancer Lett., 114, 221-223.
69. Gradelet, S., Le Bon, A.M., Berges, R., Suschetet, M. and Astorg, P. 1998. Dietary carotenoids inhibit aflatoxin B1-induced liver preneoplastic foci and DNA damage in the rat: role of the modulation of aflatoxin B1 metabolism. Carcinogenesis, 19, 403-411.
70. Gray, D.A. 1996. Carotenoids and sexual dichromatism in North American passerine birds. Am. Nat., 148, 453-480.
71. Grether, F.G., Hudon, J. and Millie, D.F. 1999. Carotenoid limitation of sexual selection along an environmental gradient in guppies. Proc. R. Soc. Lond. B, 266, 1317-1322.
72. Halliwell, B. 1996. Antioxidants in human health and disease. Annu. Rev. Nutr., 16, 33-50.
73. Hamilton, W.D. and Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites? Science, 218, 384-386.
74. Hannon, S.J. and Eason, P. 1995. Colour bands, combs and coverable badges in willow ptarmigan. Anim. Behav., 49, 53-62.
75. Hansen, A.J. and Rohwer, S. 1986. Coverable badges and resource defence in birds. Anim. Behav., 34, 69-76.
76. Haq, A., Bailey, C.A. and Chinnah, A. 1996. Effect of β-carotene, canthaxanthin, lutein, and vitamin E on neonatal immunity of chicks when supplemented in the broiler breeder diets. Poultry Sci., 75, 1092-1097
77. He, Y. and Campbell, T.C. 1990. Effects of carotenoids on aflatoxin B1-induced mutagenesis in S. typhimurium TA 100 and TA 98. Nutr. Cancer, 13, 243-253.
78. Henderson, D., Bird, D.M., Rau, M.E. and Negro, J.J. 1995. Mate choice in captive American kestrels, Falco sparverius, parasitized by a nematode, Trichinella pseudospiralis. Ethology, 101, 112-120.
79. Hill, G.E. 1990. Female house finches prefer colorful males: sexual selection for a condition-dependent trait. Anim. Behav., 40, 563-572.
80. Hill, G.E. 1991. Plumage coloration is a sexually selected indicator of male quality. Nature, 350, 337-339.
81. Hill, G.E. 1992. Proximate basis of variation in carotenoid pigmentation in male house finches. Auk, 109, 1-12.
82. Hill, G.E. 1993. Geographic variation in carotenoid plumage pigmentation of male house finches Carpodacus mexicanus. Biol. J. Linn. Soc., 49, 63-86.
83. Hill, G.E. 1994. Geographic variation in male ornamentation and female preference in the house finch: A comparative test of models of sexual selection. Behav. Ecol., 5, 64-73.
84. Hill, G.E. 1995. Seasonal variation in circulating carotenoid pigments in the house finch. Auk, 112, 1057-1061.
85. Hill, G.E. 1999. Is there an immunological cost to carotenoid-based ornamental coloration? Am. Nat., 154, 589-595.
86. Hill, G.E. and Brawner, W.R., III. 1998. Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proc. R. Soc. Lond. B, 265, 1105-1109.
87. Hill, G.E., Montgomerie, R., Roeder, C. and Boag, P. 1994a. Sexual selection and cuckoldry in a monogamous songbird: Implications for sexual selection theory. Behav. Ecol. Sociobiol., 35, 193-199.
88. Hill, G.E., Montgomerie, R., Inouye, C. and Dale, J. 1994b. Influence of dietary carotenoids on plasma and plumage color in the house finch: intra-and intersexual variation. Funct. Ecol., 8, 343-350.
89. Hill, G.E., Nolan, P.M. and Stoehr, A.M. 1999. Pairing success relative to male plumage redness and pigment symmetry in the house finch: temporal and geographic constancy. Behav. Ecol., 10, 48-53.
90. Hillgarth, N. 1990. Parasites and female choice in the ring-necked pheasant. Am. Zool., 30, 227-234.
91. Hiramoto, K., Tomiyama, S. and Kikugawa, K. 1999. Effective inhibition by beta-carotene of cellular DNA breaking induced by peroxynitrous acid. Free Radic. Res., 30, 21-27.
92. Holder, K. and Montgomerie, R. 1993. Context and consequences of comb displays by male rock ptarmigan. Anim. Behav., 45, 457-470.
93. Hörak, P., Ots, I., Vellau, H., Spottiswoode, C. and Møller, A.P. 2000a. Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia (in press).
94. Hörak, P., Vellau, H., Ots, I. and Møller, A.P. 2000b. Growth conditions affect carotenoid-based plumage colouration of Great Tit nestlings. Behav. Ecol. Sociobiol. (in press).
95. Houde, A.E. 1987. Mate choice based upon naturally occurring color-pattern variation in a guppy population. Evolution, 41, 1-10.
96. Houde, A.E. and Torio, A.J. 1992. Effect of parasitic infection on male color pattern and female choice in guppies. Behav. Ecol., 3, 346-351.
97. Hudon, J. 1991. Unusual carotenoid use by the Western tanager (Piranga ludoviciana) and its evolutionary implications. Can. J. Zool., 69, 2311-2320.
98. Iyama, T., Takasuga, A. and Azuma, M. 1996. Beta-carotene accumulation in mouse tissues and a protective role against lipid peroxidation. Int. J. Vitam. Nutr. Res., 66, 301-305.
99. Jaeschke, H. 1995. Mechanisms of oxidant stress-induced acute tissue injury. Proc. Soc. Exp. Biol. Med., 209, 104-111.
100. Jain, C.K., Agarwal, S. and Rao, A.V. 1999. The effect of dietary lycopene on bioavailability, tissue distribution, in vivo antioxidant properties and colonic preneoplasia in rats. Nutr. Res., 19, 1383-1391.
101. Jialal, I., Norkus, E.P., Cristol, L. and Grundy, S.M. 1991. Beta-carotene inhibits the oxidative modification of low-density lipoprotein. Biochim. Biophys. Acta, 1086, 134-138.
102. Johnsen, T.S. and Zuk, M. 1996. Repeatability of mate choice in female red jungle fowl. Behav. Ecol., 7, 243-246.
103. Johnson, K., Dalton, R. and Burley, N. 1993. Preferences of female American goldfinches (Carduelis tristis) for natural and artificial male traits. Behav. Ecol., 4, 138-143.
104. Jyonouchi, H., Sun, S. and Gross, M. 1995. Effect of carotenoids on in vitro immunoglobulin production by human peripheral blood mononuclear cells: astaxanthin, a carotenoid without vitamin A activity, enhances in vitro immunoglobulin production in response to a T-dependent stimulant and antigen. Nutr. Cancer, 23, 171-183.
105. Jyonouchi, H., Zhang, L., Gross, M. and Tomita, Y. 1994. Immunomodulating actions of carotenoids: enhancement of in vivo and in vitro antibody production to T-dependent antigens. Nutr. Cancer, 21, 47-58.
106. Kazanskaya, L.N., Sinyavskaya, N.D., Shabaev, S.V., Popov, V.I. and Ivnitskii, Yu.Yu. 1994. Experimental evaluation of sodium succinate and beta-carotene as radioprotective com-ponents of special grades of bread. Voprosy Pitaniya., 1-2, 23-25.
107. Kennedy, C.E.J., Endler, J.A., Poyton, S.L. and McMinn, H. 1987. Parasite load predicts mate choice in guppies. Behav. Ecol. Sociobiol., 21, 291-295.
108. Kilner, R. 1997. Mouth colour is a reliable signal of need in begging canary nestlings. Proc. R. Soc. Lond. B., 264, 963-968.
109. Kilner, R. and Johnstone, R. 1997. Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol. Evol., 12, 11-15.
110. Kim, H. 1995. Carotenoids protect cultured rat hepatocytes from injury caused by carbon tetrachloride. Int. J. Biochem. Cell. Biol, 27, 1303-1309.
111. Kim, H.P., Kim, S.Y., Lee, E.J. and Kim, Y.C. 1997. Zeaxanthin dipalmitate from Lycium chinense has hepatoprotective activity. Res. Commun. Mol. Pathol. Pharmacol., 97, 301-314.
112. Kim, H.W., Chew, B.P., Wong, T.S., Park, J.S., Weng, B.B.C., Byrne, K.M., Hayek, M.G. and Reinhart, G.A. 2000. Modulation of humoral and cell-mediated immune responses by dietary lutein in cats. Vet. Immunol. Immunopathol., 73, 331-341.
113. Kodric-Brown, A. 1985. Female preferences and sexual selection for male coloration in the guppy. Behav. Ecol. Sociobiol., 17, 199-205.
114. Kodric-Brown, A. 1989. Dietary carotenoids and male mating success in the guppy: An environmental component to female choice. Behav. Ecol. Sociobiol., 25, 393-401.
115. Korpimäki, E., Tolonen, P. and Bennett, G.F. 1995. Blood parasites, sexual selection and reproductive success of European kestrels. Ecoscience, 2, 335-343.
116. Kowalski, L.M. and Reid, W.M. 1970. Some effects of roxarsone on pigmentation of chickens infected with coccidia. Poultry Sci., 49, 1405.
117. Kraus, A., Roth, H.P. and Kirchgessner, M. 1997. Supplementation with vitamin C, vitamin E or beta-carotene influences osmotic fragility and oxidative damage of erythrocytes of zinc-deficient rats. J. Nutr., 127, 1290-1296.
118. Krinsky, N.I. 1989. Antioxidant functions of carotenoids. Free Radic. Biol. Med., 7, 617-635.
119. Krinsky, N.I. 1998. The antioxidant and biological properties of the carotenoids. Ann. N. Y. Acad. Sci., 854, 443-447.
120. Kunert, K.J. and Tappel, A.L. 1983. The effect of vitamin C on in vivo lipid peroxidation in guinea pigs as measured by pentane and ethane production. Lipids, 18, 271-274.
121. Latscha, T. 1990. Carotenoids - their nature and significance in animal feeds. F. Hoffman-LaRoche Ltd., Basel.
122. Lawlor, S.M. and O'Brien, N.M. 1995. Astaxanthin: antioxidant effects in chicken embryo fibroblasts. Nutr. Res., 15, 1695-1704.
123. Lawlor, S.M. and O'Brien, N.M. 1997. Modulation of paraquat toxicity by beta-carotene at low oxygen partial pressure in chicken embryo fibroblasts. Br. J. Nutr., 77, 133-140.
124. Leal, M., de Mejia, E.G., Ruiz, F. and Shimada, A. 1998. Effect of carotenoids on cytotoxicity of T-2 toxin on chicken hepatocytes in vitro. Toxicology in Vitro, 12, 133-139.
125. Lepage, G., Champagne, J., Ronco, N., Lamarre, A., Osberg, I., Sokol, R.J. and Roy, C.C. 1997. Supplementation with carotenoids corrects increased lipid eroxidation in children with cystic fibrosis. Am. J. Clin. Nutr., 64, 87-93.
126. Levin, G., Yeshurun, M. and Mokady, S. 1997. In vivo antiperoxidative effect of 9-cis beta-carotene compared with that of the all-trans isomer. Nutr. Cancer, 27, 293-297.
127. Levy, Y., Kaplan, M., Ben Amotz, A. and Aviram, M. 1996. Effect of dietary supplementation of beta-carotene on human monocyte-macrophage-mediated oxidation of low density lipoprotein. Isr. J. Med. Sci., 32, 473-478.
128. Lewis, D.M. 1972. Importance of face mask in species recognition and territorial behaviour in the Yellowthroat. Jack-Pine Warbler, 50, 98-109.
129. Ligon, J.D., Thornhill, R., Zuk, M. and Johnsen, K. 1990. Male-male competition, ornamentation and the role of testosterone in sexual selection in red jungle fowl. Anim. Behav., 40, 357-373.
130. Liljedal, S., Folstad, I. and Skarstein, F. 1999. Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr. Proc. R. Soc. Lond. B., 266, 1893-1898.
131. Lozano, G.A. 1994. Carotenoids, parasites, and sexual selection. Oikos, 70, 309-311.
132. Lyon, B.E., Eadie, J.M. and Hamilton, L.D. 1994. Parental choice selects for ornamental plumage in American coot chicks. Nature, 371, 240-243.
133. Martin, K.R., Failla, M.L. and Smith, J.C. Jr. 1996. Beta-carotene and lutein protect HepG2 human liver cells against oxidant-induced damage. J. Nutr., 126, 2098-2106.
134. Mateos, C. and Carranza, J. 1995. Female choice for morphological features of male ring-necked pheasants. Anim. Behav., 49, 737-748.
135. Mathews-Roth, M.M. 1986. Systemic photoprotection. Dermatol. Clin., 4, 335-339.
136. Mayne, S.T. 1996. Beta-carotene, carotenoids, and disease prevention in humans. FASEB J., 10, 690-701.
137. Mayne, S.T. and Parker, R.S. 1987. Dietary canthaxanthin as a protective agent against lipid peroxidation in biomembranes. Fed. Proc., 46, 1189.
138. Mayne, S.T. and Parker, R.S. 1989. Antioxidant activity of dietary canthaxanthin. Nutr. Cancer, 12, 225-236.
139. McPhail, J.D. 1969. Predation and the evolution of a stickleback (Gasterosteus) population. J. Fish. Res. Board Can., 26, 3183-3208.
140. McWhinney, S.L.L. and Bailey, C.A. 1989. Immunoenhancing effect of β-carotene in chicks. Poultry Sci., 68 (Suppl. 1), 94 (Abstr.).
141. Meydani, M., Martin, A., Ribayamercado, J.D., Gong, J.X., Blumberg, J.B. and Russell, R.M. 1994. Beta-carotene supplementation increases antioxidant capacity of plasma in older women. J. Nutr., 124, 2397-2403.
142. Miki, W. 1991. Biological functions and activities of animal carotenoids. Pure Appl. Chem., 63, 141-146.
143. Milinski, M. and Bakker, T.C.M. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, 344, 330-333.
144. Miller N.J., Sampson, J., Candeias, L.P., Bramley, P.M. and Rice-Evans, C.A. 1996. Antioxidant activities of carotenes and xanthophylls. FEBS Letters, 384, 240-242.
145. Mitchell, J.J., Paiva, M. and Heaton, M.B. 1999. The antioxidants vitamin E and beta-carotene protect against ethanol-induced neurotoxicity in embryonic rat hippocampal cultures. Alcohol, 17, 163-168.
146. Mobarhan, S., Bowen, P., Andersen, B., Evans, M., Stacewicz-Sapuntzakis, M., Sugerman, S., Simms, P., Lucchesi, D. and Friedman, H. 1990. Effects of beta-carotene repletion on beta-carotene absorption, lipid peroxidation, and neutrophil superoxide formation in young men. Nutr. Cancer, 14, 195-206.
147. Møller, A.P., Christe, P. and Lux, E. 1999. Parasitism, host immune function and sexual selection: A meta-analysis of parasite-mediated sexual selection. Q. Rev. Biol., 74, 3-20.
148. Møller, A.P., Dufva, R. and Erritzöe, J. 1998. Host immune function and sexual selection in birds. J. Evol. Biol., 11, 703-719.
149. Moore, M.M., Breedveld, M.W. and Autor, A.P. 1989. The role of carotenoids in preventing oxidative damage in the pigmented yeast, Rhodotorula mucilaginosa. Arch. Biochem. Biophys., 270, 419-431.
150. Nakagawa, K., Fujimoto, K. and Miyazawa, T. 1996. Beta-carotene as a high-potency antioxidant to prevent the formation of phospholipid hydroperoxides in red blood cells of mice. Biochim. Biophys. Acta, 1299, 110-116.
151. Nakagawa, K., Kang, S.D., Park, D.K., Handelman, G.J. and Miyazawa, T. 1997. Inhibition of beta-carotene and astaxanthin of NADPH-dependent microsomal phospholipid peroxidation. J. Nutr. Sci. Vitaminol., (Tokyo) 43, 345-355.
152. Nakano, T., Kanmuri, T., Sato, M. and Takeuchi, M. 1999. Effect of astaxanthin rich red yeast (Phaffia rhodozyma) on oxidative stress in rainbow trout. Biochim. Biophys. Acta., 1426, 119-125.
153. Nakano, T., Tosa, M. and Takeuchi, M. 1995. Improvement of biochemical features in fish health by red yeast and synthetic astaxanthin. J. Agric. Food Chem., 43, 1570-1573.
154. Niki, E. 1991. Antioxidant compounds. In: Chemical, Biological and Medical Aspects. (Davis, K.J., Ed.), Pergamon Press, Elmsford, NY, pp. 57-64.
155. Nolan, P.M., Hill, G.E. and Stoehr, A.M. 1998. Sex, size and plumage redness predict house finch survival in an epidemic. Proc. R. Soc. Lond. B., 265, 961-965.
156. North, J.A. and Tappel, A.L. 1997. Measuring the oxidation of heme compounds in heart homogenates from rats supplemented with dietary antioxidants. Free Radic. Biol. Med., 22, 175-184.
157. O'Connor, I. and O'Brien, N. 1998. Modulation of UVA light-induced oxidative stress by beta-carotene, lutein and astaxanthin in cultured fibroblasts. J. Dermatol. Sci., 16, 226-230.
158. Olson, V.A. and Owens, I.P.F. 1998. Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol., 13, 510-514.
159. Oshima, S., Ojima, F., Sakamoto, H., Ishiguro, Y. and Terao, J. 1996. Supplementation with carotenoids inhibits singlet oxygen-mediated oxidation of human plasma low-density lipoprotein. J. Agric. Food Chem., 44, 2306-2309.
160. Palozza, P. and Krinsky, N.I. 1992. β-Carotene and α-tocopherol are synergistic antioxidants. Arch. Biochem. Biophys., 297, 184-187.
161. Palozza, P., Luberto, C., Ricci, P., Sgarlata, E., Calviello, G. and Bartoli, G.M. 1996. Effect of beta-carotene and canthaxanthin on tert-butyl hydroperoxide-induced lipid peroxidation in murine normal and tumor thymocytes. Arch. Biochem. Biophys., 325, 145-151.
162. Park, J.S., Chew, B.P. and Wong, T.S. 1998. Dietary lutein from marigold extract inhibits mammary tumor development in BALB/c mice. J. Nutr., 128, 1650-1656.
163. Parker, G.A. and Mock, D.W. 1987. Parent-offspring conflict over clutch size. Evol. Ecol., 1, 161-174.
164. Parker, G.A., Mock, D.W. and Lamey, T.C. 1989. How selfish should stronger sibs be? Am. Nat., 133, 846-868.
165. Partali, V., Liaaen-Jensen, S., Slagsvold, T. and Lifjeld, J.T. 1987. Carotenoids in food chain studies: II. The food chain of Parus spp. monitored by carotenoid analysis. Comp. Biochem. Physiol., 87B, 885-888.
166. Peek, F.W. 1972. An experimental study of the territorial function of vocal and visual display in the male red-winged blackbird (Agelaius phoeniceus). Anim. Behav., 20, 112-118.
167. Pinchasov, Y., David, G. and Zohari, S. 1992. Dietary supplementation with xanthophyll as an effective way of identifying low-producing broiler breeder hens. Poultry Sci., 71, 1436-1441.
168. Preault, M. 1999. Stratégie d'appariement et sélection sexuelle chez le Merle noir, Turdus merula, en milieu urbain. MSc thesis, Université de Bourgogne, Dijon, France.
169. Prohaszka, L. 1966. The role of carotenoids and vitamin A in encephalomalacia. Br. J. Nutr., 20, 533-540.
170. Putnam, M. 1992. A review of the nature, function, variability, and supply of pigments in salmonid fish. In Aquaculture and the environment, eds. Depauw, N. and Joyce, J. European Aquaculture Society, Gent, pp. 245-263.
171. Rao, A.V. and Agarwal, S. 1998. Bioavailability and in vivo antioxidant properties of lycopene from tomato products and their possible role in the prevention of cancer. Nutr. Cancer. Intern. J., 31, 199-203.
172. Rao, A.V. and Agarwal, S. 1999. Role of lycopene as antioxidant carotenoid in the prevention of chronic diseases: a review. Nutr. Res., 19, 305-323.
173. Rauscher, R., Edenharder, R. and Platt, K.L. 1998. in vitro antimutagenic and in vivo anticlastogenic effects of carotenoids and solvent extracts from fruits and vegetables rich in carotenoids. Mutat. Res., 413, 129-142
174. Rice-Evans, C.A., Sampson, J., Bramley, P.M. and Holloway, D.E. 1997. Commentary: why do we expect carotenoids to be antioxidants in vivo. Free Radical Res., 26, 381-398.
175. Riso, P., Pinder, A., Santangelo, A. and Porrini, M. 1999. Does tomato consumption effectively increase the resistance of lymphocyte DNA to oxidative damage? Am. J. Clin. Nutr., 69, 712-718.
176. Rohwer, S. and Røskaft, E. 1989. Results of dying male yellow-headed blackbirds solid black: Implications for the arbitrary identity badge hypothesis. Behav. Ecol. Sociobiol., 25, 39-48.
177. Rose, M. E. 1981. Lymphatic system. In Form and function in birds. Vol. 2, Eds King, A. S. and McLelland, J. Academic Press, London, pp. 341-384.
178. Røskaft, E. and Rohwer, S. 1987. An experimental study of the function of the red epaulettes and the black body colour of male red-winged blackbirds. Anim. Behav., 35, 1070-1077.
179. Rowland, W.J. 1982. The effects of male nuptial coloration on stickleback aggression: A reexamination. Behaviour, 80, 118-126.
180. Ruff, M.D., Reid, W.M. and Johnson, J.K. 1974. Lowered blood carotenoid levels in chickens infected with coccidia. Poultry Sci., 53, 1801-1809.
181. Ruiz, J.A., Perez-Vendrell, A.M. and Esteve-Garcia, E. 1999. Effect of beta-carotene and vitamin E on oxidative stability in leg meat of broilers fed different supplemental fats. J. Agric. Food Chem., 47, 448-454.
182. Rust, P., Eichler, I., Renner, S. and Elmadfa, I. 1998. Effects of long-term oral beta-carotene supplementation on lipid peroxidation in patients with cystic fibrosis. Int. J. Vitam. Nutr. Res., 68, 83-87.
183. Saino, N., Stradi, R., Ninni, P. and Møller, A.P. 1999. Carotenoid plasma concentration, immune profile and plumage ornamentation of male barn swallows (Hirundo rustica). Am. Nat., 154, 441-448.
184. Saino, N., Ninni, P., Calza, S., De Bernardi, F. and Møller, A.P. 2000. Better red than dead: carotenoid-based gape coloration reveals health status in barn swallow nestlings. Proc. R. Soc. Lond. B., 267, 57-61.
185. Schaeffer, J.L. and Hamilton, P.B. 1990. Effect of dietary lipid on lutein metabolism during aflatoxicosis in young broiler chickens. Poultry Sci., 69, 53-59.
186. Schaeffer, J.L., Tyczkowsky, J., Parkhurst, C.R. and Hamilton, P.B. 1988. Carotenoid composition of serum and egg yolk of hens fed diets varying in carotenoid composition. Poultry Sci., 67, 608-614.
187. Schall, J.J. 1986. Prevalence and virulence of a haemogregarine parasite of the Aruban whiptail lizard, Cnemidophorus arubensis. J. Herpetol., 20, 318-324.
188. Schall, J.J. and Dearing, M.D. 1987. Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidentalis. Oecologia, 73, 389-392.
189. Scheidt, K. 1989. New aspects of carotenoid metabolism in animals. In Carotenoids: chemistry and biology, Eds Krinsky, N.I., Mathews-Roth, M.M. and Taylor, R.F. Plenum Press, New York, pp. 247-268.
190. Semler, D.E. 1971. Some aspects of adaptation in a polymorphism for breeding colours in the threespine stickleback (Gasterosteus aculeatus). J. Zool. Lond., 165, 291-302.
191. Seutin, G. 1994. Plumage redness in redpoll finches does not reflect hemoparasitic infection. Oikos, 70, 280-286.
192. Shykoff, J.A. and Widmer, A. 1996. Parasites and signal brightness: how general should the relationship be? Naturwissenschaften, 83, 113-121.
193. Sies, H. (Ed.) 1997. Antioxidants in disease mechanisms and therapy. San Diego and London, Academic Press.
194. Skarstein, F. and Folstad, I. 1996. Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos, 76, 359-367.
195. Slagsvold, T. and Lifjeld, J.T. 1985. Variation in plumage color of the great tit Parus major in relation to habitat, season and food. J. Zool., Lond., 206, 321-328.
196. Smith, D.G. 1972. The role of epaulets in the red-winged blackbird, Agelaius phoeniceus social system. Behaviour, 41, 251-267.
197. Someya, K., Totsuka, Y., Murakoshi, M., Kitano, H. and Miyazawa, T. 1994. The effect of natural carotenoid (palm fruit carotene) intake on skin lipid peroxidation in hairless mice. J. Nutr. Sci. Vitaminol., 40, 303-314.
198. Speake, B.K., Murray, A.M.B. and Noble, R.C. 1998. Transport and transformation of yolk lipids during development of the avian embryo. Prog. Lipid. Res., 37, 1-32.
199. Stahl, W., Junghans, A., De Boer, B., Driomina, E.S., Briviba, K. and Sies, H. 1998. Carotenoid mixture protect multilamellar liposomes against oxidative damage: synergistic effects of lycopene and lutein. FEBS Letters, 427, 305-308.
200. Stahl, W. and Sies, H. 1999. Carotenoids: occurrence, biochemical activities, and bioavailability. In Antioxidant food supplements in human health., Eds Packer, L., Hiramatsu, M. and Yoshikawa, T. Academic Press, San Diego, pp. 183-202.
201. Stradi, R. 1998. The colour of flight. Solei Gruppo Editoriale Informatico, Milan.
202. Sundberg, J. 1995a. Female yellowhammers (Emberiza citrinella) prefer yellower males: a laboratory experiment. Behav. Ecol. Sociobiol., 37, 275-282.
203. Sundberg, J. 1995b. Parasites, plumage coloration and reproductive success in the yellowhammer, Emberiza citrinella. Oikos, 74, 331-339.
204. Sundberg, J. and Dixon, A. 1996. Old, colourful male yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim. Behav., 52, 113-122.
205. Surai P. 1999. Vitamin E in avian reproduction. Poultry Avian Biol. Rev., 10, 1-60
206. Surai, P.F., Ionov, I., Kuchmistova, E., Noble, R.C. and Speake, B.K. 1998. The relationship between the levels of α-tocopherol and carotenoids in the maternal feed, yolk and neonatal tissues: comparison between the chicken, turkey, duck and goose. J. Sci. Food Agric., 76, 593-598.
207. Surai, P.F., McDevitt, R., Speake, B.K. and Sparks, N.H.C. 1999. Carotenoid distribution in tissues of the laying hen depending on their dietary supplementation. Proc. Nutr. Soc., 58, 30A.
208. Surai, P.F., Noble, R.C. and Speake, B.K. 1996. Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochem. Biophys. Acta., 1304, 1-10.
209. Surai, P.F., Royle, N.K. and Sparks, N.H.C. 2000. Fatty acid, carotenoid and vitamin A composition of tissues of free living gulls. Comp. Biochem. Physiol., (Submitted).
210. Surai, P.F. and Speake, B.K. 1998. Distribution of carotenoids from the yolk to the tissues of the developing embryo. J. Nutr. Biochem., 9, 645-651.
211. Tengerdy, R.P., Lacetera, N.G. and Nockels, C.F. 1990. Effect of beta carotene on disease protection and humoral immunity in chickens. Avian Dis., 34, 848-854.
212. Thompson, C.W., Hillgarth, N., Leu, M. and McClure, H.E. 1997. High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am. Nat., 149, 270-294.
213. Umegaki, K., Takeuchi, N., Ikegami, S. and Ichikawa, T. 1994. Effect of beta-carotene on spontaneous and X-ray-induced chromosomal damage in bone marrow cells of mice. Nutr. Cancer, 22, 277-284.
214. van Poppel, G., Spanhaak, S. and Ockhuizen, T. 1993. Effect of β-carotene on immunological indexes in healthy male smokers. Am. J. Clin. Nutr., 57, 402-407.
215. Verhulst, S., Dieleman, S.J. and Parmentier, H.K. 1999. A trade-off between immunocompetence and sexual ornamentation in chickens. Proc. Natl. Acad. Sci. USA, 96, 4478-4481.
216. Verlhac, V., Gabaudan, J. and Schierle, J. 1995. Influence of astaxanthin on non-specific immune response of rainbow trout. The Nordic Symposium on Fish Immunology, May 1995, Reykjavik, Iceland.
217. Vile, G.F. and Winterbourn, C. C. 1988. Inhibition of adriamycin-promoted microsomal lipid peroxidation by beta-carotene, alpha-tocopherol and retinol at high and low oxygen partial pressures. FEBS Lett., 238, 353-356.
218. Vleck, C.M. and Bucher, T.L. 1998 Energy metabolism, gas exchange, and ventilation. In Avian growth and development: evolution within the altricial-precocial spectrum, Eds Starck, J.M. and Ricklefs, R.E. Oxford University Press, Oxford, pp. 89-116.
219. von Schantz, T., Tufvesson, M., Göransson, G., Grahn, M., Wilhelmson, M. and Wittzell, H. 1995. Artificial selection for increased comb size and its effects on other sexual characters and viability in Gallus domesticus (the domestic chicken). Heredity, 75, 518-529.
220. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. and Wittzell, H. 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B., 266, 1-12.
221. Watson, R.R., Prabhala, R.H., Plezia, P.M. and Alberts, D.S. 1991. Effects of β-carotene on lymphocyte subpopulations in elderly humans: Evidence for a dose-response relationship. Am. J. Clin. Nutr., 53, 90-94.
222. Weatherhead, P. and Boag, P.T. 1995. Pair and extra-pair success relative to male quality in red-winged blackbirds. Behav. Ecol. Sociobiol., 37, 81-91.
223. Weatherhead, P.J., Metz, K.J., Bennett, G.F. and Irwin, R.E. 1993. Parasites fauna, testosterone and secondary sexual traits in male red-winged blackbirds. Behav. Ecol. Sociobiol., 33, 13-23.
224. Weitberg, A.B., Weitzman, S.A., Clark, E.P. and Stossel, T.P. 1985. Effects of antioxidants on oxidant-induced sister chromatid exchange formation. J. Clin. Invest., 75, 1835-1841.
225. Whittaker, P., Wamer, W.G., Chanderbhan, R.F. and Dunkel, V.C. 1996. Effects of alpha-tocopherol and beta-carotene on hepatic lipid peroxidation and blood lipids in rats with dietary iron overload. Nutr. Cancer, 25, 119-128.
226. Wiehn, J., Korpimäki, E., Bildstein, K.L. and Sorjonen, J. 1997. Mate choice and reproductive success in the American kestrel: a role for blood parasites? Ethology, 103, 304-317.
227. Winklhofer-Roob, B.M., Puhl, H., Khoschsorur, G., van't Hof, M.A., Esterbauer, H. and Shmerling, D.H. 1995. Enhanced resistance to oxidation of low density lipoproteins and decreased lipid peroxide formation during beta-carotene supplementation in cystic fibrosis. Free Radic. Biol. Med., 18, 849-859.
228. Winklhofer-Roob, B.M., Schlegel-Haueter, S.E., Khoschsorur, G., van't Hof, M.A., Suter, S. and Shmerling, D.H. 1996. Neutrophil elastase/alpha1-proteinase inhibitor complex levels decrease in plasma of cystic fibrosis patients during long-term oral beta-carotene supplementation. Pediatric Res., 40, 130-134.
229. Wolfenbarger, L.L. 1999. Red coloration of male northern cardinals correlates with mate quality and territory quality. Behav. Ecol., 10, 80-90.
230. Woodall, A.A., Britton, G. and Jackson, M.J. 1996. Dietary supplementation with carotenoids: effects on α-tocopherol levels and susceptibility of tissues to oxidative stress. Brit. J. Nutr., 76, 307-317.
231. Yezerinac, S.M. and Weatherhead, P.J. 1997. Extra-pair mating, male plumage coloration and sexual selection in yellow warblers (Dendroica petechia). Proc. R. Soc. Lond. B., 264, 527-532.
232. Yvore, P. and Mainguy, P. 1972. Influence de la coccidiose duodenale sur la teneur en carotenoides du serum chez le poulet. Ann. Rech. Vet., 3, 381-387.
233. Zamora, R., Hidalgo, F.J. and Tappel, A.L. 1991. Comparative antioxidant effectiveness of dietary beta-carotene, vitamin E, selenium and coenzyme Q10 in rat erythrocytes and plasma. J. Nutr., 121, 50-56.
234. Zhang, L.X., Cooney, R.V. and Bertram, J.S. 1991. Carotenoids enhance gap junctional communication and inhibit lipid peroxidation in C3H/10T1/2 cells: relationship to their cancer chemopreventive action. Carcinogenesis, 12, 2109-2114.
235. Zuk, M. and Johnsen, T.S. 1998. Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc. R. Soc. Lond. B., 265, 1631-1635.
236. Zuk, M., Johnson, K., Thornhill, R. and Ligon, J.D. 1990a. Mechanisms of female choice in red jungle fowl. Evolution, 44, 477-485.
237. Zuk, M., Johnson, K., Thornhill, R. and Ligon, J.D. 1990b. Parasites and male ornaments in free-ranging and captive red jungle fowl. Behaviour, 14, 232-248.
238. Zuk, M., Thornhill, R., Ligon, J. and Johnson, K. 1990d. Parasites and mate choice in red jungle fowl. Am. Zool., 30, 235-244.
239. Zuk, M., Thornhill, R., Ligon, J.D., Johnson, K., Austad, S., Ligon, S.H., Thornhill, N.W. and Costin, C. 1990c. The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am. Nat., 136, 459-473.
240. Zuk, M., Ligon, J.D. and Thornhill, R. 1992. Effects of experimental manipulation of male secondary sexual characters on female mate choice preference in red jungle fowl. Anim. Behav., 44, 999-1006.
241. Zuk, M., Johnsen, T.S. and MacLarty, T. 1995. Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc. R. Soc. Lond. B., 260, 205-210.