Abstract
Melanin-based variation in colour patterns is under strong genetic control and not, or weakly, sensitive to the environment and body condition. Current signalling theory predicts that such traits may not signal honestly phenotypic quality because their production does not entail a significant fitness cost. However, recent studies revealed that in several bird species melanin-based traits covary with phenotypic attributes. In a first move to understand whether such covariations have a physiological basis, we quantified concentrations of five chemical elements in two pigmented plumage traits in the barn owl (Tyto alba). This bird shows continuous variation from immaculate to heavily marked with black spots (plumage spottiness) and from dark reddish-brown to white (plumage coloration), two traits that signal various aspects of individual quality. These two traits are sexually dimorphic with females being spottier and darker coloured than males. We found an enhancement in calcium and zinc concentration within black spots compared with the unspotted feather parts. The degree to which birds were spotted was positively correlated with calcium concentration within spots, whereas the unspotted feather parts of darker reddish-brown birds were more concentrated in zinc. This suggests that two different pigments are responsible for plumage spottiness and plumage coloration. We discuss the implications of our results in light of recent experimental field studies showing that female spottiness signals offspring humoral response towards an artificially administrated antigen, parasite resistance and fluctuating asymmetry of wing feathers.
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References
Andersson M (1994) Sexual selection. Princeton University Press, Princeton, N.J.
Badyaev AV, Hill GE (2000) Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol J Linn Soc 69:153–172
Barsh GS (1996) The genetics of pigmentation: from fancy genes to complex traits. Trends Genet 12:299–305
Baudvin H (1975) Biologie de reproduction de la chouette effraie (Tyto alba) en Côte d'Or: premiers résultats. Jean Blanc 14:1–51
Bogacz A, Buszman E, Wilczok T (1989) Competition between metal ions for dopa-melanin. Stud Biophys 132:189–195
Bowers RR, Biboso A, Chavez O (1997) The role of alpha-MSH, its agonists, and C-AMP in vitro avian melanocytes. Pigment Cell Res 10:41–45
Buckley PA (1987) Mendelian genes. In: Cooke F, Buckley PA (eds) Avian genetics, a population and ecological approach. Academic Press, London, pp 1–44
Burger J (1994) Metal in avian feathers: bioindicators of environmental pollution. Res Environ Toxicol 26:351–355
Catania A, Cutuli M, Garofalo L, Carlin A, Airaghi L, Barcellini W, Lipton JM (2000) The neuropeptide α-MSH in host defense. Ann NY Acad Sci 917:227–231
Chen H, Hayakawa D, Emura S, Ozawa Y, Okumura T, Shoumara S (2002) Effect of low or high dietary calcium on the morphology of the rat femur. Histol Histopathol 17:1129–1135
Goede AA (1985) Mercury, selenium, arsenic and zinc in waders from the dutch Wadden Sea. Environ Pollut A37:287–309
Hartner L, Huebner N, Schreiber N (1992) Über die Eignung der Vogelfeder als Bioindikator. Hohenheimer Umwelttagung 24:75–91
Hearing VJ, Tsukamoto K (1991) Enzymatic control of pigmentation in mammals. FASEB J 5:2902–2909
Hill GE, Brawner WR (1998) Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proc R Soc Lond B 265:1105–1109
Hurwitz S (1989) Calcium homeostasis in birds. Vitam Horm 45:173–221
Ichiyama T, Sato S, Okada K, Catania A, Lipton JM (2000) The neuroimmunomodulatory peptide α-MSH. Ann NY Acad Sci 917:221–226
Lerner AB, McGuire JS (1961) Effect of alpha- and beta-melanocyte stimulating hormones on the skin colour of man. Nature 189:176–179
Majerus MEN (1998) Melanism, Evolution in action. Oxford University Press, Oxford
Matics R, Hoffmann G, Nagy T, Roulin A (2002) Random pairing with respect to plumage coloration in Hungarian barn owls. J Ornithol 143:493–495
McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:1525–1531
Mountjoy K, Kong PL, Willars DH, Wilkinson WO (2001) Melanocortin receptor-mediated mobilization of intracellular free calcium in HEK 293 cells. Physiol Genom 5:11–19
Murton RK, Westwood NJ, Thearle RJP (1973) Polymorphism and the evolution of continuous breeding season in the pigeon Columba livia. J Reprod Fertil [Suppl] 19:561–575
Niecke M (1999) Ist die selektive Anreicherung von Elementen in melaninhaltigen Vogelfedern ein generelles Phänomen? Beitr Gefiederkd Morphol Vögel 6:36–43
Niecke M, Ambor S, Kühnast O, Ellenberg H (1990a) Vogelfedern als Biomonitoren für die atmosphärischeSchwermetallbelastung Untersuchungen mit der Protonenmikrosonde, Teil I. Externe Deposition von Schwermetallen auf Elsternfedern. UmweltwissSchadstoff-Forschung 2:71–75
Niecke M, Ambor S, Kühnast O, Ellenberg H (1990b) Vogelfedern als Biomonitoren für die atmosphärischeSchwermetallbelastung Untersuchungen mit der Protonenmikrosonde, Teil II. Die mikroskopische Verteilung von Schwermetallen auf Elsternfedern. UmweltwissSchadstoff-Forschung 4:188–192
Okazaki K, Kuwata K, Miki Y, Shiga S, Shiga T (1985) Electron spin relaxation of synthetic melanin and melanin-containing human tissues as studied by electron spin echo and electron spin resonance. Arch Biochem Biophys 242:197–205
Price T, Bontrager A (2001) The evolution of plumage patterns. Curr Biol 11:405–408
Prota G (1992) Melanins and Melanogenesis. Academic Press London
Rohwer S, Rohwer FC (1978) Status signalling in harris sparrows: experimental deceptions achieved. Anim Behav 26, 1012–1022
Roulin A (1999a) Delayed maturation of plumage coloration and spottiness in the barn owl Tyto alba. J Ornithol 140:193–197
Roulin A (1999b) Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait. Behav Ecol 10:688–695
Roulin A, Dijkstra C (2003) Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90:359–364
Roulin A, Richner H, Ducrest A-L (1998) Genetic, environmental and condition-dependent effects on female and male ornamentation in the barn owl Tyto alba. Evolution 52:1451–1460
Roulin A, Ducrest A-L, Dijkstra C (1999) Effects of brood size manipulations on parents and offspring in the barn owl, Tyto alba. Ardea 87:91–100
Roulin A, Jungi TW, Pfister H, Dijkstra C (2000) Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B 267:937–941
Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001a) Female- and male-specific signals of quality in the barn owl. J Evol Biol 14:255–267
Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001b) Female plumage spottiness and parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110
Roulin A, Ducrest A-L, Balloux F, Dijkstra C, Riols C (2003) A female melanin-ornament signals offspring fluctuating asymmetry in the barn owl. Proc R Soc Lond B 270:167–171
Salceda R, Sanchez-Chavez G (2000) Calcium uptake, release and ryanodine binding in melanosomes from retinal pigment epithelium. Cell Calcium 27:223–229
Sánchez-Ferrer á, Rodriguez-López JN, García-Cánovas F, García-Carmona F (1995) Tyrosinase: a comprehensive review of its mechanism. Biochem Biophys Acta 1247:1–11
Scanlon PF, O´Brien TG, Schauer NL, Coggin JL, Steffen DE (1979) Heavy metal levels in feathers of wild turkeys from Virginia. Bull Environ Contam Toxicol 21:591
Scanlon PF, Oderwald RG, Dietrick TJ, Coggin JL (1980) Heavy metal concentration in feathers of Ruffed Grouse shot by Virginian hunters. Bull Environ Contam Toxicol 25:947–949
Stettenheim P (1972) The integument of birds In: King F (ed) Avian biology II. Academic Press, New York, pp 1–63
Wilkinson L (1989) SYSTAT: the system for statistics. SYSTAT, Evanston, Ill.
Acknowledgements
We thank Anne-Lyse Ducrest, the late Martin Epars and Henri Etter for their help during the fieldwork and Willy Rehpenning for his help in accelerator maintenance. Pierre Bize, Anne-Lyse Ducrest and two anonymous referees provided useful comments on a first draft of this paper. Fieldwork was under the legal authorisation of the Service vétérinaire du canton de Vaud. A.R. was supported by a grant of the Swiss Science Foundation (grant no. 823A-064710). We are grateful to Cor Dijkstra and Guido Meeuwissen for having sexed nestlings using the CHD method.
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An erratum to this article can be found at http://dx.doi.org/10.1007/s00442-003-1341-1
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Niecke, M., Rothlaender, S. & Roulin, A. Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers. Oecologia 137, 153–158 (2003). https://doi.org/10.1007/s00442-003-1307-3
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DOI: https://doi.org/10.1007/s00442-003-1307-3