Carotenoids and skin coloration in a social raptor

Journal of Raptor Research

Volumn 47, Issue 2, 2013, Pages 174-184

  Blas, Julio ^a   Cabezas, Sonia ^b   Figuerola, Jordi ^a   López, Lidia ^a   Tanferna, Alessandro ^a   Hiraldo, Fernando ^a   Sergio, Fabrizio ^a   Negro, Juan J ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Black Kite; carotenoids; coloration; constraint; dominance; Milvus migrans; restraint; sexual selection; status signaling

Indexed keywords

CAROTENOID; COLOR; COMPETITION (ECOLOGY); DOMINANCE; PHYSIOLOGY; PIGMENT; PLASMA; RAPTOR; REPRODUCTIVE BEHAVIOR; SEXUAL SELECTION; SIGNALING; SKIN;

EID: 84877837542     PISSN: 08921016     EISSN: None     Source Type: Journal    
DOI: 10.3356/JRR-12-46.1     Document Type: Article

References (74)

1. ALONSO-A LVAREZ, C., S. BERTRAND, G. DEVEVEY, M. GAILLARD, J. PROSA, B. FAIVRE, AND G. SORCI. 2004. An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. American Naturalist 164: 651-659. (Pubitemid 39509014)
2. (Pubitemid 47056761)
3. ANDERSSON, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ U.S.A.
4. ANDERSSON, S. AND M. PRAGER. 2006. Quantifying colors. Pages 78 in G.E. Hill and K.J. McGraw [EDS.], Bird coloration, Vol. 2: function and evolution. Harvard Univ. Press, Cambridge, MA U.S.A.
5. ARMSTRONG, G.A. AND J.E. HEARST. 1996. Carotenoids 2: Genetics and molecular biology of carotenoid pigment biosynthesis. FASEB Journal 10: 228-237. (Pubitemid 26079942)
6. BLAS, J. AND F. HIRALDO. 2010. Proximate and ultimate factors explaining floating behavior in long-lived birds. Hormones and Behavior 57: 169-176.
7. -, L. LO PEZ, A. TANFERNA, F. SERGIO, AND F. HIRALDO. 2010. Reproductive endocrinology of wild, long-lived raptors. General and Comparative Endocrinology 168: 22-28.
8. (Pubitemid 44913462)
9. -, F. SERGIO, AND F. HIRALDO. 2009. Age-related improvement in reproductive performance in a long-lived raptor: a cross-sectional and longitudinal study. Ecography 32: 647-657.
10. -,-, J.C. WINGFIELD, AND F. HIRALDO. 2011. Experimental tests of endocrine function in breeding and nonbreeding raptors. Physiological and Biochemical Zoology 84: 406-416.
11. BLOUNT, J.D., D.C. HOUSTON, AND A.P. MØLLER. 2000. Why egg yolk is yellow. Trends in Ecology and Evolution 15: 47-49. (Pubitemid 30349800)
12. (Pubitemid 36423043)
13. BORTOLOTTI, G.R., K.J. FERNIE, AND J.E. SMITS. 2003. Carotenoid concentration and coloration of American Kestrels (Falco sparverius) disrupted by experimental exposure to PCBs. Functional Ecology 17: 651-657. (Pubitemid 37274342)
14. -, J.J. NEGRO, J.L. TELLA, T.A. MARCHANT, AND D.M. BIRD. 1996. Sexual dichromatism in birds independent of diet, parasites and androgens. Proceedings of the Royal Society of London Series B 263: 1171-1176.
15. (Pubitemid 30612372)
16. BOSTROM, M.R. AND G. RITCHISON. 2006. Possible relationships between morphology, territory quality, and skin color of American Kestrels. Journal of Field Ornithology 4: 392-398. (Pubitemid 44760161)
17. BRADBURY, J.W. AND S.L. VEHRENCAMP. 2011. Principles of animal communication. Sinauer, Sunderland, MA.
18. BRUSH, A.H. 1981. Carotenoids in wild and captive birds. Pages 539-562 in J.C. Baurenfeind [ED.], Carotenoids as colorants and vitamin A precursors. Academic Press, New York, NY U.S.A.
19. -. 1990. Metabolism of carotenoid pigments in birds. FASEB Journal 4: 2969-2977.
20. BUSTAMANTE, J. AND F. HIRALDO. 1989. Post-fledging dependence period and maturation of flight skills in the Black Kite Milvus migrans. Bird Study 36: 199-204. (Pubitemid 20423373)
21. CASAGRANDE, S., D. COSTANTINI, A. FANFANI, J. TAGLIAVINI, AND G. DELL'OMO. 2007. Patterns of serum carotenoid accumulation and skin color variation in kestrel nestlings in relation to breeding conditions and different terms of carotenoid supplementation. Journal of Comparative Physiology B 177: 237-245. (Pubitemid 46185099)
22. (Pubitemid 43356942)
23. -, G. DELL'OMO, D. CONSTANTINI, J. TAGLIAVINI, AND T. GROOTHUIS. 2011. Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian Kestrel: a multi-factorial study. Comparative Biochemistry and Physiology A 160: 16-26.
24. CHEW, B.P. AND J.S. PARK. 2004. Carotenoid action on the immune response. Journal of Nutrition 134: 257S-261.
25. CONSTANTINI, D. AND A.P. MØLLER. 2008. Carotenoids are minor antioxidants for birds. Functional Ecology 22: 367-370. (Pubitemid 351416629)
26. -, M. ROWE, M.W. BUTLER, AND K.J. MCGRAW. 2010. From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Functional Ecology 24: 950-959.
27. CRAMP, S. AND K.E.L. SIMMONS. 1980. The birds of the western palearctic, Vol. 2: Hawks to bustards. Oxford Univ. Press, Oxford, U.K.
28. CURIO, E. 1983. Why do young birds reproduce less well? Ibis 125: 400-404. (Pubitemid 15275957)
29. DARWIN, C. 1871. The descent of man, and selection in relation to sex. John Murray, London, U.K.
30. DAWSON, R.D. AND G.R. BORTOLOTTI. 2006. Carotenoid-dependent coloration of male American Kestrels predicts ability to reduce parasitic infections. Naturwissenschaften 93: 597-602. (Pubitemid 44819301)
31. DEL HOYO, J., A. ELLIOTT, AND J. SARGATAL. 1994. Handbook of the birds of the world, Vol. 2. New World vultures to guineafowl. Lynx Editions, Barcelona, Spain.
32. DESROCHERS, A. 1992. Age-related differences in reproduction by European Blackbirds: restraint or constraint? Ecology 73: 1128-1131.
33. ELLEGREN, H. 1996. First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proceedings of the Royal Society of London Series B 263: 1635-1641. (Pubitemid 27055555)
34. FAIVRE, B., A. GREGOIRE, M. PREAULT, F. CEZILLY, AND G. SORCI. 2003. Immune activation rapidly mirrored in a secondary sexual trait. Science 300: 103. (Pubitemid 36423036)
35. FIGUEROLA, J., E. MUN OZ, R. GUTIE RREZ, AND D. FERRER. 1999. Blood parasites, leucocytes and plumage brightness in the Cirl Bunting Emberiza cirlus. Functional Ecology 13: 594-601.
36. FOLSTAD, I. AND A.J. KARTER. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist 139: 603-622.
37. FORERO, M.G., J.A. DONA ZAR, J. BLAS, AND F. HIRALDO. 1999. Causes and consequences of territory change and breeding dispersal distance in the Black Kite. Ecology 80: 1298-1310. (Pubitemid 29279933)
38. GERARD, L., G.L. HAWKINS, AND G.E. HILL. 2012. Delayed plumage maturation and delayed reproductive investment in birds. Biological Reviews 87: 257-274.
39. KNOWLES, S.C., L.S. NAKAWAHE, AND B.C. SHELDON. 2009. Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a metaregression approach. Functional Ecology 23: 405-515.
40. LAAKSONEN, T., J.J. NEGRO, S. LYYTINEN, J. VALKAMA, I. OTS, AND E. KORPIMAKI. 2008. Effects of experimental brood size manipulation and gender on carotenoid levels of Eurasian Kestrels Falco tinnunculus. PLoS ONE 3(6): e2374. doi: 10.1371/journal.pone.0002374.
41. LANDIS, J.R. AND G.G. KOCH. 1977. Themeasurement of observer agreement for categorical data. Biometrics 33: 159-174. (Pubitemid 8054849)
42. MARTINEZ-PADILLA, J., F. MOUGEOT, L. PE REZ-RODRIGUEZ, AND G.R. BORTOLOTTI. 2007. Nematode parasites reduce carotenoid-based signalling in male Red Grouse. Biology Letters 3: 161-164. (Pubitemid 351878143)
43. MATEOS, C. AND J. CARRANZA. 1997. The role of bright plumage in male-male interactions in the Ring-necked Pheasant. Animal Behaviour 54: 1205-1214. (Pubitemid 27518874)
44. MAYNARD SMITH, J. AND D. HARPER. 2003. Animal signals. Oxford Univ. Press, Oxford, U.K.
45. MCCULLAGH, P. AND J.A. NELDER. 1989. Generalized linear models. Chapman and Hall, New York, NY U.S.A.
46. MCDONALD, P.G. 2003. Variable plumage and bare part colouration in the Brown Falcon, Falco berigora: the influence of age and sex. Emu 103: 21-28. (Pubitemid 36530822)
47. MCGRAW, K.J. AND G.E.HILL. 2006. Mechanics of carotenoidbased colouration. Pages 177-242 in G.E. Hill and K.J. McGraw [EDS.], Bird coloration, Vol. 2: Function and evolution. Harvard Univ. Press, Cambridge, MA U.S.A.
48. MØLLER, A.P., C. BIARD, J.D. BLOUNT, D.C. HOUSTON, P. NINNI, N. SAINO, AND P.F. SURAI. 2000. Carotenoid dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian and Poultry Biology Reviews 11: 137-159.
49. MONTGOMERIE, R. 2006. Analyzing colors. Pages 113 in G.E. Hill and K.J. McGraw [EDS.], Bird coloration, Vol. 2: Function and evolution. Harvard Univ. Press, Cambridge, MA U.S.A.
50. MOUGEOT, F. AND B. ARROYO. 2006. Ultraviolet reflectance in the cere of raptors. Biology Letters 2: 173-176.
51. (Pubitemid 32100789)
52. MUNSELL, A.H. 1912. A pigment color system and notation. American Journal of Psychology 23: 236-244.
53. NEGRO, J.J., G.R. BORTOLOTTI, J.L. TELLA, K.J. FERNIE, AND D.M. BIRD. 1998. Regulation of integumentary colour and plasma carotenoids in American Kestrels consistent with sexual selection theory. Functional Ecology 12: 307-312. (Pubitemid 28276222)
54. -, J.M. GRANDE, J.L. TELLA, J.L. GARRIDO, D. HORNERO, J.A. DONAZAR, J.A. Sanchez-ZAPATA, J.R. BENITEZ, AND M. BARCELL. 2002. Coprophagy: an unusual source of essential carotenoids-a Yellow-faced Vulture includes ungulate faeces in its diet for cosmetic purposes. Nature 416: 807-808.
55. NEWTON, I. AND P. ROTHERY. 2001. Estimation and limitation of numbers of floaters in a Eurasian Sparrowhawk population. Ibis 143: 442-449. (Pubitemid 32554662)
56. PENTERIANI, V., M. FERRER, AND M.M. DELGADO. 2011. Floater strategies and dynamics in birds, and their importance in conservation biology: towards an understanding of nonbreeders in avian populations. Animal Conservation 14: 233-241.
57. PEREZ-RODRIGUEZ, L. 2008. Carotenoid-based ornamentation as a dynamic but consistent individual trait. Behavioral Ecology and Sociobiology 62: 995-1005.
58. SARASOLA, J.H., J.J. NEGRO, M.J. BECHARD, AND A. LANUSSE. 2011. Not as similar as thought: sexual dichromatism in Chimango Caracaras is expressed in the exposed skin but not in the plumage. Journal of Ornithology 152: 473-479.
59. SERGIO, F., J. BLAS, R. BAOS, M.G. FORERO, J.A. DONAZAR, AND F. HIRALDO. 2009b. Short and long-term consequences of individual and territory quality in a longlived bird. Oecologia 160: 507-514.
60. -,-, G. BLANCO, A. TANFERNA, L. LO PEZ, J.A. LEMUS, AND F. HIRALDO. 2011a. Raptor nest decorations are a reliable threat against conspecifics. Science 331: 327-330.
61. (Pubitemid 350150763)
62. (Pubitemid 47357649)
63. -,-, AND F. HIRALDO. 2009a. Predictors of floater status in a long-lived bird: a cross-sectional and longitudinal test of hypotheses. Journal of Animal Ecology 78: 109-118.
64. -, G. TAVECCHIA, J. BLAS, L. LO PEZ, A. TANFERNA, AND F. HIRALDO. 2011b. Variation in age-structured vital rates of a long-lived raptor: implications for population growth. Basic and Applied Ecology 12: 107-115.
65. STEENHOF, K. AND B. PETERSON. 2009. Site fidelity, mate fidelity, and breeding dispersal in American Kestrels. Wilson Journal of Ornithology 121: 12-21.
66. STERNALSKI, A., F. MOUGEOT, AND V. BRETAGNOLLE. 2012. Carotenoid limitation and allocation priorities in asynchronous raptor nestlings. Biological Journal of the Linnean Society 105: 13-24.
67. -,-, C. ERAUD, B. GANGLOFF, A. VILLERS, AND V. BRETAGNOLLE. 2010. Carotenoids in nestling Montagu's Harriers: variations according to age, sex, body-condition and evidence for diet-related limitations. Journal of Comparative Physiology B 180: 33-43.
68. STUDD, M.V. AND R.J. ROBERTSON. 1985. Evidence for reliable badges of status in territorial Yellow Warblers (Dendroica petechia). Animal Behaviour 33: 1102-1113.
69. VERGARA, P. AND J.A. FARGALLO. 2011. Multiple coloured ornaments in male common kestrels: different mechanisms to convey quality. Naturwissenschaften 98: 289-298.
70. VILLAGE, A. 1985. Turnover, age and sex ratios of kestrels (Falco tinnunculus) in south Scotland. Journal of Zoology 206: 175-189.
71. WIERSMA, P., C. SELMAN, J.R. SPEAKMAN, AND S. VERHULST. 2004. Birds sacrifice oxidative protection for reproduction. Biology Letters 271: S360-S363. (Pubitemid 38998748)
72. ZACK, S. AND B.J. STUTCHBURY. 1992. Delayed breeding in avian social systems: the role of territory quality and 'floater' tactics. Behaviour 123: 194-219. (Pubitemid 24406803)
73. ZAHAVI, A. 1975. Mate selection-a selection for a handicap. Journal of Theoretical Biology 53: 205-214.
74. ZUUR, A.F., E.N. LENO, N.J. WALKER, A.A. SAVELIEV, AND G.M. SMITH. 2007. Mixed effects models and extensions in ecology with R. Springer, New York, NY U.S.A.