, Volume 5, Issue 3, pp 328–337 | Cite as

Environmental Pollution Affects the Plumage Color of Great Tit Nestlings through Carotenoid Availability

  • Tapio Eeva
  • Saila Sillanpää
  • Juha-Pekka Salminen
  • Lauri Nikkinen
  • Anu Tuominen
  • Eija Toivonen
  • Kalevi Pihlaja
  • Esa Lehikoinen


Birds need to acquire carotenoids for their feather pigmentation from their diet, which means that their plumage color may change as a consequence of human impact on their environment. For example, the carotenoid-based plumage coloration of Great tit, Parus major, nestlings is associated with the degree of environmental pollution. Breast feathers of birds in territories exposed to heavy metals are less yellow than those in unpolluted environments. Here we tested two hypotheses that could explain the observed pattern: (I) deficiency of carotenoids in diet, and (II) pollution-related changes in transfer of carotenoids to feathers. We manipulated dietary carotenoid levels of nestlings and measured the responses in plumage color and tissue concentrations. Our carotenoid supplementation produced the same response in tissue carotenoid concentrations and plumage color in polluted and unpolluted environments. Variation in heavy metal levels did not explain the variation in tissue (yolk, plasma, and feathers) carotenoid concentrations and was not related to plumage coloration. Instead, the variation in plumage yellowness was associated with the availability of carotenoid-rich caterpillars in territories. Our results support the hypothesis that the primary reason for pollution-related variation in plumage color is carotenoid deficiency in the diet.


carotenoids bioindicator heavy metal pollution oxidative stress Parus major plumage color 


  1. Aykin-Burns N, Laegeler A, Kellogg G, Erca N (2003) Oxidative effects of lead in young and adult fisher 344 rats. Archives of Environmental Contamination and Toxicology 44:417–420CrossRefGoogle Scholar
  2. Biard C, Surai PF, Møller AP (2005) Effects of carotenoid availability during laying on reproduction in the blue tit. Oecologia 144:32–44CrossRefGoogle Scholar
  3. Blount JD (2004) Carotenolds and life-history evolution in animals. Archives of Biochemistry and Biophysics 430:10–15CrossRefGoogle Scholar
  4. Blount JD, Houston DC, Møller AP (2000) Why egg yolk is yellow. Trends in Ecology and Evolution 15:47–49CrossRefGoogle Scholar
  5. Brush AH (1978) Avian pigmentation. In: Chemical Zoology, Brush AH (editor), New York: Academic Press, pp 141–164Google Scholar
  6. Edge R, McGarvey DJ, Truscott TG (1997) The carotenoids as anti-oxidants—a review. Journal of Photochemistry and Photobiology B: Biology 41:189–200CrossRefGoogle Scholar
  7. Eeva T, Lehikoinen E (2000) Improved breeding success in forest passerines after decreased emissions of heavy metals. Nature 403:851–852CrossRefGoogle Scholar
  8. Eeva T, Lehikoinen E, Nikinmaa M (2003) Pollution-induced nutritional stress in birds: an experimental study of direct and indirect effects. Ecological Applications 13:1242–1249CrossRefGoogle Scholar
  9. Eeva T, Lehikoinen E, Pohjalainen T (1997) Pollution-related variation in food supply and breeding success in two hole-nesting passerines. Ecology 78:1120–1131CrossRefGoogle Scholar
  10. Eeva T, Lehikoinen E, Rönkä M (1998) Air pollution fades the plumage of the great tit. Functional Ecology 12:607–612CrossRefGoogle Scholar
  11. Eeva T, Ryömä M, Riihimäki J (2005) Pollution-related changes in diets of two insectivorous passerines. Oecologia 145:629–639CrossRefGoogle Scholar
  12. Fair J, Whitaker S, Pearson B (2007) Sources of variation in hematocrit in birds. Ibis 149:535–552CrossRefGoogle Scholar
  13. Fitze PS, Kölliker M, Richner H (2003a) Effects of common origin and common environment on nestling plumage coloration in the great tit (Parus major). Evolution 57:144–150Google Scholar
  14. Fitze PS, Tschirren B, Richner H (2003b) Carotenoid-based colour expression is determined early in nestling life. Oecologia 137:148–152CrossRefGoogle Scholar
  15. Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. Journal of Avian Biology 31:559–566CrossRefGoogle Scholar
  16. Hõrak P, Ots I, Vellau H, Spottiswoode C, Møller AP (2001) Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126:166–173CrossRefGoogle Scholar
  17. Hõrak P, Surai PF, Møller AP (2002) Fat-soluble antioxidants in the eggs of great tits Parus major in relation to breeding habitat and laying sequence. Avian Science 2:123–130Google Scholar
  18. Isaksson C, McLaughlin P, Monaghan P, Andersson S (2007) Carotenoid pigmentation does not reflect total non-enzymatic antioxidant activity in plasma of adult and nestling great tits, Parus major. Functional Ecology 21:1123–1129CrossRefGoogle Scholar
  19. Isaksson C, Örnborg J, Stephensen E, Andersson S (2005) Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits. EcoHealth 2:138–146CrossRefGoogle Scholar
  20. Johnsen A, Delhey K, Andersson S, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proceedings of the Royal Society of London. Series B: Biological Sciences 270:1263–1270CrossRefGoogle Scholar
  21. Kiikkilä O (2003) Heavy-metal pollution and remediation of forest soil around the Harjavalta Cu-Ni smelter, in SW Finland. Silva Fennica 37:399–415Google Scholar
  22. Krinsky NI, Yeum KJ (2003) Carotenoid-radical interactions. Biochemical and Biophysical Research Communications 305:754–760CrossRefGoogle Scholar
  23. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121Google Scholar
  24. Mateo R, Hoffman DJ (2001) Differences in oxidative stress between young Canada geese and mallards exposed to lead-contaminated sediment. Journal of Toxicology and Environmental Health—Part A 64:531–545CrossRefGoogle Scholar
  25. McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Bird Coloration I: Mechanisms and Measurements, Hill GE, McGraw KJ (editors), Boston: Harvard University Press, pp 177–242Google Scholar
  26. McGraw KJ, Hill GE, Stradi R, Parker RS (2001) The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Cardinalis cardinalis). Physiological and Biochemical Zoology 74:843–852CrossRefGoogle Scholar
  27. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N et al (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian and Poultry Biology Reviews 11:137–159Google Scholar
  28. Montgomerie R (2006) Analysing colors. In: Bird Coloration, Hill GE, McGraw KJ (editors), Boston: Harvard University Press, pp 90–147Google Scholar
  29. Partali V, Liaaen-Jensen S, Slagsvold T, Lifjeld JT (1985) Carotenoids in food chain studies—II. The food chain of Parus spp. monitored by carotenoid analysis. Comparative Biochemistry and Physiology B—Comparative Biochemistry and Molecular Biology 82:767–772CrossRefGoogle Scholar
  30. Perrins CM (1965) Population fluctuations and clutch-size in the great tit, Parus major L. Journal of Animal Ecology 34:601–647CrossRefGoogle Scholar
  31. Polidori MC, Stahl W, Eichler O, Niestroj I, Sies H (2001) Profiles of antioxidants in human plasma. Free Radical Biology and Medicine 30:456–462CrossRefGoogle Scholar
  32. Rönkä M (1999) The plumage colour of the great tit (Parus major) nestlings along an air pollution gradient. MSc Thesis, University of Turku, FinlandGoogle Scholar
  33. Royle NJ, Surai PF, McCartney RJ, Speake BK (1999) Parental investment and egg yolk lipid composition in gulls. Functional Ecology 13:298–306CrossRefGoogle Scholar
  34. Senar JC, Figuerola J, Domenech J (2003) Plumage coloration and nutritional condition in the great tit Parus major: the roles of carotenoids and melanins differ. Naturwissenschaften 90:234–237Google Scholar
  35. Shawkey MD, Hill GE (2005) Carotenoids need structural colours to shine. Biology Letters 1:121–124CrossRefGoogle Scholar
  36. Shawkey MD, Hill GE, McGraw KJ, Hood WR, Huggins K (2006) An experimental test of the contributions and condition dependence of microstructure and carotenoids in yellow plumage coloration. Proceedings of the Royal Society of London. Series B: Biological Sciences 273:2985–2991CrossRefGoogle Scholar
  37. Slagsvold T, Lifjeld JT (1985) Variation in plumage colour of the great tit Parus major in relation to habitat, season and food. Journal of Zoology (London) 206:321–328Google Scholar
  38. Stehbens WE (2003) Oxidative stress, toxic hepatitis, and antioxidants with particular emphasis on zinc. Experimental and Molecular Pathology 75:265–276CrossRefGoogle Scholar
  39. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal-ions. Free Radical Biology and Medicine 18:321–336CrossRefGoogle Scholar
  40. Tschirren B, Fitze PS, Richner H (2003) Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.). Journal of Evolutionary Biology 16:91–100CrossRefGoogle Scholar
  41. Tschirren B, Fitze PS, Richner H (2005) Carotenoid-based nestling colouration and parental favouritism in the great tit. Oecologia 143:477–482CrossRefGoogle Scholar
  42. Villafuerte R, Negro JJ (1998) Digital imaging for colour measurement in ecological research. Ecology Letters 1:151–154CrossRefGoogle Scholar
  43. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proceedings of the Royal Society of London. Series B: Biological Sciences 266:1–12CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2008

Authors and Affiliations

  • Tapio Eeva
    • 1
  • Saila Sillanpää
    • 1
  • Juha-Pekka Salminen
    • 2
  • Lauri Nikkinen
    • 1
  • Anu Tuominen
    • 2
  • Eija Toivonen
    • 1
  • Kalevi Pihlaja
    • 2
  • Esa Lehikoinen
    • 1
  1. 1.Section of EcologyUniversity of TurkuTurkuFinland
  2. 2.Laboratory of Organic Chemistry and Chemical BiologyUniversity of TurkuTurkuFinland

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