, Volume 137, Issue 1, pp 153–158 | Cite as

Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers

  • Manfred Niecke
  • Sven Rothlaender
  • Alexandre RoulinEmail author
Behavioural Ecology


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.


Calcium Genetic colour polymorphism Immunocompetence Tyto alba Zinc 



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.


  1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, N.J.Google Scholar
  2. Badyaev AV, Hill GE (2000) Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol J Linn Soc 69:153–172CrossRefGoogle Scholar
  3. Barsh GS (1996) The genetics of pigmentation: from fancy genes to complex traits. Trends Genet 12:299–305CrossRefPubMedGoogle Scholar
  4. Baudvin H (1975) Biologie de reproduction de la chouette effraie (Tyto alba) en Côte d'Or: premiers résultats. Jean Blanc 14:1–51Google Scholar
  5. Bogacz A, Buszman E, Wilczok T (1989) Competition between metal ions for dopa-melanin. Stud Biophys 132:189–195Google Scholar
  6. Bowers RR, Biboso A, Chavez O (1997) The role of alpha-MSH, its agonists, and C-AMP in vitro avian melanocytes. Pigment Cell Res 10:41–45PubMedGoogle Scholar
  7. Buckley PA (1987) Mendelian genes. In: Cooke F, Buckley PA (eds) Avian genetics, a population and ecological approach. Academic Press, London, pp 1–44Google Scholar
  8. Burger J (1994) Metal in avian feathers: bioindicators of environmental pollution. Res Environ Toxicol 26:351–355Google Scholar
  9. 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 917:227–231PubMedGoogle Scholar
  10. 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 17:1129–1135PubMedGoogle Scholar
  11. Goede AA (1985) Mercury, selenium, arsenic and zinc in waders from the dutch Wadden Sea. Environ Pollut A37:287–309Google Scholar
  12. Hartner L, Huebner N, Schreiber N (1992) Über die Eignung der Vogelfeder als Bioindikator. Hohenheimer Umwelttagung 24:75–91Google Scholar
  13. Hearing VJ, Tsukamoto K (1991) Enzymatic control of pigmentation in mammals. FASEB J 5:2902–2909PubMedGoogle Scholar
  14. Hill GE, Brawner WR (1998) Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proc R Soc Lond B 265:1105–1109CrossRefGoogle Scholar
  15. Hurwitz S (1989) Calcium homeostasis in birds. Vitam Horm 45:173–221PubMedGoogle Scholar
  16. Ichiyama T, Sato S, Okada K, Catania A, Lipton JM (2000) The neuroimmunomodulatory peptide α-MSH. Ann NY Acad Sci 917:221–226PubMedGoogle Scholar
  17. Lerner AB, McGuire JS (1961) Effect of alpha- and beta-melanocyte stimulating hormones on the skin colour of man. Nature 189:176–179Google Scholar
  18. Majerus MEN (1998) Melanism, Evolution in action. Oxford University Press, OxfordGoogle Scholar
  19. Matics R, Hoffmann G, Nagy T, Roulin A (2002) Random pairing with respect to plumage coloration in Hungarian barn owls. J Ornithol 143:493–495Google Scholar
  20. McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:1525–1531CrossRefPubMedGoogle Scholar
  21. Mountjoy K, Kong PL, Willars DH, Wilkinson WO (2001) Melanocortin receptor-mediated mobilization of intracellular free calcium in HEK 293 cells. Physiol Genom 5:11–19Google Scholar
  22. Murton RK, Westwood NJ, Thearle RJP (1973) Polymorphism and the evolution of continuous breeding season in the pigeon Columba livia. J Reprod Fertil [Suppl] 19:561–575Google Scholar
  23. Niecke M (1999) Ist die selektive Anreicherung von Elementen in melaninhaltigen Vogelfedern ein generelles Phänomen? Beitr Gefiederkd Morphol Vögel 6:36–43Google Scholar
  24. 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 2:71–75Google Scholar
  25. 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 4:188–192Google Scholar
  26. 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 242:197–205PubMedGoogle Scholar
  27. Price T, Bontrager A (2001) The evolution of plumage patterns. Curr Biol 11:405–408CrossRefPubMedGoogle Scholar
  28. Prota G (1992) Melanins and Melanogenesis. Academic Press LondonGoogle Scholar
  29. Rohwer S, Rohwer FC (1978) Status signalling in harris sparrows: experimental deceptions achieved. Anim Behav 26, 1012–1022Google Scholar
  30. Roulin A (1999a) Delayed maturation of plumage coloration and spottiness in the barn owl Tyto alba. J Ornithol 140:193–197Google Scholar
  31. Roulin A (1999b) Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait. Behav Ecol 10:688–695CrossRefGoogle Scholar
  32. Roulin A, Dijkstra C (2003) Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90:359–364CrossRefPubMedGoogle Scholar
  33. 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 52:1451–1460Google Scholar
  34. Roulin A, Ducrest A-L, Dijkstra C (1999) Effects of brood size manipulations on parents and offspring in the barn owl, Tyto alba. Ardea 87:91–100Google Scholar
  35. Roulin A, Jungi TW, Pfister H, Dijkstra C (2000) Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B 267:937–941CrossRefPubMedGoogle Scholar
  36. Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001a) Female- and male-specific signals of quality in the barn owl. J Evol Biol 14:255–267CrossRefGoogle Scholar
  37. Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001b) Female plumage spottiness and parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110CrossRefGoogle Scholar
  38. 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 270:167–171CrossRefPubMedGoogle Scholar
  39. Salceda R, Sanchez-Chavez G (2000) Calcium uptake, release and ryanodine binding in melanosomes from retinal pigment epithelium. Cell Calcium 27:223–229CrossRefPubMedGoogle Scholar
  40. Sánchez-Ferrer á, Rodriguez-López JN, García-Cánovas F, García-Carmona F (1995) Tyrosinase: a comprehensive review of its mechanism. Biochem Biophys Acta 1247:1–11PubMedGoogle Scholar
  41. 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 21:591PubMedGoogle Scholar
  42. 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 25:947–949PubMedGoogle Scholar
  43. Stettenheim P (1972) The integument of birds In: King F (ed) Avian biology II. Academic Press, New York, pp 1–63Google Scholar
  44. Wilkinson L (1989) SYSTAT: the system for statistics. SYSTAT, Evanston, Ill.Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Manfred Niecke
    • 1
  • Sven Rothlaender
    • 1
  • Alexandre Roulin
    • 2
    Email author
  1. 1.Institut für ExperimentalphysikUniversität Hamburg HamburgGermany
  2. 2.Department of ZoologyUniversity of CambridgeCambridgeUK

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