, Volume 188, Issue 3, pp 683–693 | Cite as

Solar and terrestrial radiations explain continental-scale variation in bird pigmentation

  • Ismael GalvánEmail author
  • Alberto Jorge
  • Carlos Pacheco
  • Derek Spencer
  • Duncan J. Halley
  • Christian Itty
  • Jan Kornan
  • Jan T. Nielsen
  • Tuomo Ollila
  • Gunnar Sein
  • Marian Stój
  • Juan J. Negro
Physiological ecology - original research


Animals living on the earth’s surface are protected from the damaging effects of solar ultraviolet (UV) radiation by melanin pigments that color their integument. UV levels that reach the earth’s surface vary spatially, but the role of UV exposure in shaping clinal variations in animal pigmentation has never been tested. Here, we show at a continental scale in Europe that golden eagles Aquila chrysaetos reared in territories with a high solar UV-B radiation exposure deposit lower amounts of the sulphurated form of melanin (pheomelanin) in feathers and consequently develop darker plumage phenotypes than eagles from territories with lower radiation exposure. This clinal variation in pigmentation is also explained by terrestrial γ radiation levels in the rearing territories by a similar effect on the pheomelanin content of feathers, unveiling natural radioactivity as a previously unsuspected factor shaping animal pigmentation. These findings show for the first time the potential of solar and terrestrial radiations to explain pigmentation phenotype diversity in animals, including humans, at large spatial scales.


Animal coloration Melanins Natural radioactivity Pigmentation UV radiation 



IG is supported by a Ramón y Cajal Fellowship (RYC-2012-10237) from the Spanish Ministry of Economy and Competitiveness (MINECO). We thank Jānis Ķuze, Carl Knoff, Peter L. Pap and Gabriel Banderet for field work in Latvia, Norway, Romania and Switzerland, respectively. Metod Macek and Anton Sedlak helped with field work in Slovakia. Ulf Johansson provided us with samples from the Swedish Museum of Natural History. Rafael Márquez helped with the spectrophotometric analyses of feathers. T. Szegvary kindly allowed us to use their map of terrestrial γ-dose rates for Europe. Four reviewers commented on the manuscript.

Author contribution statement

IG conceived the study, contributed to sampling, analyzed the data and wrote the manuscript. AJ conducted the analyses of Raman spectroscopy. CP, DS, DJH, CI, JK, JTN, TO, GS and MS contributed to sampling. JJN contributed to sampling and manuscript writing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of animal rights

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2018_4238_MOESM1_ESM.pdf (64 kb)
Supplementary material 1 (PDF 64 kb)
442_2018_4238_MOESM2_ESM.pdf (523 kb)
Supplementary material 2 (PDF 523 kb)


  1. Alcaide M, Serrano D, Tella JL, Negro JJ (2009) Strong phylopatry derived from capture–recapture records does not lead to fine-scale genetic differentiation in lesser kestrels. J Anim Ecol 78:468–475CrossRefGoogle Scholar
  2. Beckmann M, Václavík T, Manceur AM, Šprtová L, Wehrden H, Welk E, Cord AF (2014) glUV: a global UV-B radiation data set for macroecological studies. Methods Ecol Evol 5:372–383CrossRefGoogle Scholar
  3. Bivand R, Keitt T, Rowlingson B (2017) rgdal: Bindings for the geospatial data abstraction library. R package version 1.2–8. Available at:
  4. Bräuner EV, Loft S, Sørensen M, Jensen A, Andersen CE, Ulbak K, Hertel O, Pedersen C, Tjønneland A, Kjær SK, Raaschou-Nielsen O (2015) Residential radon exposure and skin cancer incidence in a prospective Danish cohort. PLoS One 10:e0135642CrossRefGoogle Scholar
  5. Brenner M, Hearing VJ (2008) The protective role of melanin against UV damage in human skin. Photochem Photobiol 84:539–549CrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach. Springer-Verlag, New YorkGoogle Scholar
  7. Comont D, Martinez Abaigar J, Albert A, Aphalo P, Causton DR, Figueroa FL, Gaberscik A, Llorens L, Hauser M-T, Jansen MAK, Kardefelt M, de la Coba Luque P, Neubert S, Núñez-Olivera E, Olsen J, Robson M, Schreiner M, Sommaruga R, Strid Å, Torre S, Turunen M, Veljovic-Jovanovic S, Verdaguer D, Vidovic M, Wagner J, Winkler JB, Zipoli G, Gwynn-Jones D (2012) UV responses of Lolium perenne raised along a latitudinal gradient across Europe: a filtration study. Physiol Plant 145:604–618CrossRefGoogle Scholar
  8. Comont D, Winters A, Gomez LD, McQueen-Mason SJ, Gwynn-Jones D (2013) Latitudinal variation in ambient UV-B radiation is an important determinant of Lolium perenne forage production, quality, and digestibility. J Exp Bot 64:2193–2204CrossRefGoogle Scholar
  9. Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  10. Crombie IK (1979) Variation of melanoma incidence with latitude in North America and Europe. Br J Cancer 40:774–781CrossRefGoogle Scholar
  11. D’Orazio JA, Nobuhisa T, Cui R, Arya M, Spry M, Wakamatsu K, Igras V, Kunisada T, Granter SR, Nishimura EK et al (2006) Topical drug rescue strategy and skin protection based on the role of Mc1r in UV-induced tanning. Nature 443:340–344CrossRefGoogle Scholar
  12. Dadachova E, Casadevall A (2008) Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol 11:525–531CrossRefGoogle Scholar
  13. Del Bino S, Ito S, Sok J, Nakanishi Y, Bastien P, Wakamatsu K, Bernerd F (2015) Chemical analysis of constitutive pigmentation of human epidermis reveals constant eumelanin to pheomelanin ratio. Pigment Cell Melanoma Res 28:707–717CrossRefGoogle Scholar
  14. Fargallo JA, Laaksonen T, Korpimäki E, Wakamatsu K (2007) A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol Ecol 21:157–171CrossRefGoogle Scholar
  15. Ferguson-Lees J, Christie DA (2001) Raptors of the world. Helm, LondonGoogle Scholar
  16. Forster L, Forster P, Lutz-Bonengel S, Willkomm H, Brinkmann B (2002) Natural radioactivity and human mitochondrial DNA mutations. Proc Natl Acad Sci USA 99:13950–13954CrossRefGoogle Scholar
  17. Fransson T, Kolehmainen T, Kroon C, Jansson L, Wenninger T (2010) EURING list of longevity records for European birds. Available at:
  18. Galván I (2017) Condition-dependence of pheomelanin-based coloration in nuthatches Sitta europaea suggests a detoxifying function: implications for the evolution of juvenile plumage patterns. Sci Rep 7:9138CrossRefGoogle Scholar
  19. Galván I, Alonso-Alvarez C (2011) Natural radioactivity can explain clinal variation in the expression of melanin-based traits. Evol Ecol 25:1197–1203CrossRefGoogle Scholar
  20. Galván I, Jorge A (2015) Dispersive Raman spectroscopy allows the identification and quantification of melanin types. Ecol Evol 5:1425–1431CrossRefGoogle Scholar
  21. Galván I, Solano F (2016) Bird integumentary melanins: biosynthesis, forms, function and evolution. Int J Mol Sci 17:520CrossRefGoogle Scholar
  22. Galván I, Wakamatsu K (2016) Color measurement of the animal integument predicts the content of specific melanin forms. RSC Adv 6:79135–79142CrossRefGoogle Scholar
  23. Galván I, Bijlsma RG, Negro JJ, Jarén M, Garrido-Fernández J (2010) Environmental constraints for plumage melanization in the northern goshawk Accipiter gentilis. J Avian Biol 41:523–531CrossRefGoogle Scholar
  24. Galván I, Ghanem G, Møller AP (2012) Has removal of excess cysteine led to the evolution of pheomelanin? BioEssays 34:565–568CrossRefGoogle Scholar
  25. Galván I, Jorge A, Ito K, Tabuchi K, Solano F, Wakamatsu K (2013) Raman spectroscopy as a non-invasive technique for the quantification of melanins in feathers and hairs. Pigment Cell Melanoma Res 26:917–923CrossRefGoogle Scholar
  26. Galván I, Bonisoli-Alquati A, Jenkinson S, Ghanem G, Wakamatsu K, Mousseau TA, Møller AP (2014) Chronic exposure to low-dose radiation at Chernobyl favours adaptation to oxidative stress in birds. Funct Ecol 28:1387–1403CrossRefGoogle Scholar
  27. Galván I, Jorge A, García-Gil M (2017a) Pheomelanin molecular vibration is associated with mitochondrial ROS production in melanocytes and systemic oxidative stress and damage. Integr Biol 9:751–761CrossRefGoogle Scholar
  28. Galván I, Inácio Â, Romero-Haro AA, Alonso-Alvarez C (2017b) Adaptive downregulation of pheomelanin-related Slc7a11 gene expression by environmentally induced oxidative stress. Mol Ecol 26:849–858CrossRefGoogle Scholar
  29. Hansson LA, Hylander S, Sommaruga R (2007) Escape from UV threats in zooplankton: a cocktail of behavior and protective pigmentation. Ecology 88:1932–1939CrossRefGoogle Scholar
  30. Hijmans RJ, van Etten J (2016) raster: Geographic data analysis and modeling. R package version 2.5-8. Available at:
  31. Hofer R, Mokri C (2000) Photoprotection in tadpoles of the common frog, Rana temporaria. Photochem Photobiol 59:48–53CrossRefGoogle Scholar
  32. Hsiung BK, Blackledge TA, Shawkey MD (2015) Spiders do have melanin after all. J Exp Biol 218:3632–3635CrossRefGoogle Scholar
  33. Hsu SL, Moore WH, Krimm S (1976) Vibrational spectrum of the unordered polypeptide chain: a Raman study of feather keratin. Biopolymers 15:1513–1528CrossRefGoogle Scholar
  34. Hull JM, Anderson R, Bradbury M, Estep JA, Ernest HB (2008) Population structure and genetic diversity in Swainson’s Hawks (Buteo swainsoni): implications for conservation. Cons Gen 9:305CrossRefGoogle Scholar
  35. Ito S, Nakanishi Y, Valenzuela RK, Brilliant MH, Kolbe L, Wakamatsu K (2011) Usefulness of alkaline hydrogen peroxide oxidation to analyze eumelanin and pheomelanin in various tissue samples: application to chemical analysis of human hair melanins. Pigment Cell Melanoma Res 24:605–613CrossRefGoogle Scholar
  36. Jablonski NG, Chaplin G (2010) Human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci USA 107(Suppl. 2):8962–8968CrossRefGoogle Scholar
  37. Kim E, Panzella L, Micillo R, Bentley WE, Napolitano A, Payne GF (2015) Reverse engineering applied to red human hair pheomelanin reveals redox-buffering as a pro-oxidant mechanism. Sci Rep 5:18447CrossRefGoogle Scholar
  38. Lowe C, Goodman-Lowe G (1996) Suntanning in hammerhead sharks. Nature 383:677CrossRefGoogle Scholar
  39. Marionnet C, Pierrard C, Golebiewski C, Bernerd F (2014) Diversity of biological effects induced by longwave UVA rays (UVA1) in reconstructed skin. PLoS One 9:e105263CrossRefGoogle Scholar
  40. Megía-Palma R, Jorge A, Reguera S (2018) Raman spectroscopy reveals the presence of both eumelanin and pheomelanin in the skin of lacertids. J Herpetol 52(1):67–73CrossRefGoogle Scholar
  41. Mitra D, Luo X, Morgan A, Wang J, Hoang MP, Lo J, Guerrero CR, Lennerz JK, Mihm MC, Wargo JA et al (2012) An ultraviolet-radiation-independent pathway to melanoma carcinogenesis in the red hair/fair skin background. Nature 491:449–453CrossRefGoogle Scholar
  42. Møller AP, Mousseau TA (2013) The effects of natural variation in background radioactivity on humans, animals and other organisms. Biol Rev 88:226–254CrossRefGoogle Scholar
  43. Morgan AM, Lo J, Fisher DE (2013) How does pheomelanin synthesis contribute to melanomagenesis? BioEssays 35:672–676CrossRefGoogle Scholar
  44. Napolitano A, Panzella L, Monfrecola G, d’Ischia M (2014) Pheomelanin-induced oxidative stress: bright and dark chemistry bridging red hair phenotype and melanoma. Pigment Cell Melanoma Res 27:721–733CrossRefGoogle Scholar
  45. Neyfakh EA, Alimbekova AI, Ivanenko GF (1998) Radiation-induced lipoperoxidative stress in children coupled with deficit of essential antioxidants. Biochemistry (Moscow) 63:977–987Google Scholar
  46. Nybakken L, Aubert S, Bilger W (2004) Epidermal UV-screening of arctic and alpine plants along a latitudinal gradient in Europe. Polar Biol 27:391–398CrossRefGoogle Scholar
  47. Panzella L, Leone L, Greco G, Vitiello G, D’errico G, Napolitano A, d’Ischia M (2014) Red human hair pheomelanin is a potent pro-oxidant mediating UV-independent contributory mechanisms of melanomagenesis. Pigment Cell Melanoma Res 27:244–252CrossRefGoogle Scholar
  48. Pavel S, Smit NPM, Pizinger K (2011) Dysplastic nevi as precursor melanoma lesions. In: Borovanský J, Riley PA (eds) Melanins and melanosomes: biosynthesis, biogenesis, physiological, and pathological functions. Wiley-Blackwell, Weinheim, pp 383–393CrossRefGoogle Scholar
  49. Peteya JA, Clarke JA, Li Q, Gao KQ, Shawkey MD (2017) The plumage and colouration of an enantiornithine bird from the Early Cretaceous of China. Palaeontology 60:55–71CrossRefGoogle Scholar
  50. Phillips RL, Cummings JL, Berry JD (1991) Responses of breeding golden eagles to relocation. Wildl Soc Bull 19:430–434Google Scholar
  51. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: Linear and nonlinear mixed effects models. R package version 3.1-131. Available at:
  52. Polidori C, Jorge A, Ornosa C (2017) Eumelanin and pheomelanin are predominant pigments in bumblebee (Apidae: Bombus) pubescence. PeerJ 5:e3300CrossRefGoogle Scholar
  53. Poston JP, Hasselquist D, Stewart IRK, Westneat DF (2005) Dietary amino acids influence plumage traits and immune responses of male house sparrows, Passer domesticus, but not as expected. Anim Behav 70:1171–1181CrossRefGoogle Scholar
  54. Riley PA (1994) Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65:27–33CrossRefGoogle Scholar
  55. Sarkar AK (2004) An evaluation of UV protection imparted by cotton fabrics dyed with natural colorants. BMC Dermatol 4:15CrossRefGoogle Scholar
  56. Schreiber RW, Schreiber EA, Peele AM, Burtt EH Jr (2006) Pattern of damage to albino Great Frigatebird flight feathers supports hypothesis of abrasion by airborne particles. Condor 108:736–741CrossRefGoogle Scholar
  57. Seckmeyer G, Pissulla D, Glandorf M, Henriques D, Johnsen B, Webb A, Siani A-M, Bais A, Kjeldstad B, Brogniez C, Lenoble J, Gardiner B, Kirsch P, Koskela T, Kaurola J, Uhlmann B, Slaper H, den Outer P, Janouch M, Werle P, Gröbner J, Mayer B, de la Casiniere A, Simic S, Carvalho F (2008) Variability of UV irradiance in Europe. Photochem Photobiol 84:172–179PubMedGoogle Scholar
  58. Spycher BD, Lupatsch JE, Zwahlen M, Röösli M, Niggli F, Grotzer MA, Rischewski J, Egger M, Kuehni CE, for the Swiss Pediatric Oncology Group and the Swiss National Cohort (2015) Background ionizing radiation and the risk of childhood cancer: a census-based nationwide cohort study. Environ Health Perspect 123:622–628CrossRefGoogle Scholar
  59. Swann HK (1924) On the races of the golden eagle (Aquila chrysaëtos). Bull Br Orn Club 45:64–73Google Scholar
  60. Szegvary T, Conen F, Stöhlker U, Dubois G, Bossew P, de Vries G (2007) Mapping terrestrial & γ-dose rate in Europe based on routine monitoring data. Radiat Meas 42:1561–1572CrossRefGoogle Scholar
  61. Takaki Y, Kawahara T, Kitamura H, Endo K-I, Kudo T (2009) Genetic diversity and genetic structure of northern goshawk Accipiter gentilis populations in eastern Japan and central Asia. Cons Genet 10(269):279Google Scholar
  62. Tao Z, Zha Y, Akiba S, Sun Q, Zou J, Li J, Liu Y, Kato H, Sugahara T, Wei L (2000) Cancer mortality in the high background radiation areas of Yangjiang, China during the period between 1979 and 1995. J Rad Res 41(Suppl):S31–S41CrossRefGoogle Scholar
  63. Vernet M, Diaz SB, Fuenzalida HA, Camilion C, Booth CR, Cabrera S, Casiccia C, Deferrari G, Lovengreen C, Paladini A, Pedroni J, Rosales A, Zagarese H (2009) Quality of UVR exposure for different biological systems along a latitudinal gradient. Photochem Photobiol Sci 8:1329–1345CrossRefGoogle Scholar
  64. Wang C, Han XS, Li FF, Huang S, Qin YW, Zhao XX, Jing Q (2016a) Forkhead containing transcription factor Albino controls tetrapyrrole-based body pigmentation in planarian. Cell Disc 2:16029CrossRefGoogle Scholar
  65. Wang H, Osseiran S, Igras V, Nichols AJ, Roider EM, Pruessner J, Tsao H, Fisher DE, Evans CL (2016b) In vivo coherent Raman imaging of the melanomagenesis-associated pigment pheomelanin. Sci Rep 6:37986CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ismael Galván
    • 1
    Email author
  • Alberto Jorge
    • 2
  • Carlos Pacheco
    • 3
  • Derek Spencer
    • 4
  • Duncan J. Halley
    • 5
  • Christian Itty
    • 6
  • Jan Kornan
    • 7
  • Jan T. Nielsen
    • 8
  • Tuomo Ollila
    • 9
  • Gunnar Sein
    • 10
  • Marian Stój
    • 11
    • 12
  • Juan J. Negro
    • 1
  1. 1.Department of Evolutionary EcologyDoñana Biological Station, CSICSevilleSpain
  2. 2.Laboratory of Non-Destructive Analytical TechniquesNational Museum of Natural Sciences, CSICMadridSpain
  3. 3.LisbonPortugal
  4. 4.Centre for Mountain StudiesUniversity of the Highlands and IslandsPerthScotland, UK
  5. 5.Norwegian Institute for Nature Research (NINA)TrondheimNorway
  6. 6.National Hunting and Wildlife Agency, Regional Delegation of OccitanieToulouseFrance
  7. 7.Administration of Protected Landscape Area of KysuceČadcaSlovakia
  8. 8.SindalDenmark
  9. 9.Metsähallitus, Parks & WildlifeRovaniemiFinland
  10. 10.Eagle ClubPõlvamaaEstonia
  11. 11.Magura National ParkKrempnaPoland
  12. 12.Eagle Conservation CommitteeJasloPoland

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