Behavioral Ecology and Sociobiology

, Volume 61, Issue 5, pp 741–751 | Cite as

Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse

  • F. Mougeot
  • J. Martínez-Padilla
  • L. Pérez-Rodríguez
  • G. R. Bortolotti
Original Article


Among the most familiar sexual signals are red, yellow, and orange sexual traits pigmented by carotenoids. Many birds can detect near-ultraviolet (UV) light, and UV signals can play key roles in mate choice. Grouse (Tetraonidae) exhibit bright carotenoid-dependent sexual ornaments, their supra-orbital combs, which to humans appear orange-red. Combs also reflect in the UV, which is not visible to humans but is likely to be visible to grouse. In male red grouse Lagopus lagopus scoticus, we show that comb UV reflectance decreases with increasing comb size and redness. By removing the epidermis of combs, where carotenoid pigments are, we show that the UV reflectance is a property of the dermis, underneath the red pigmented epidermis. Carotenoid pigmentation of combs acted as a mask to reduce reflectance by the dermis in the range 400–550 nm and in the UV, 300–400 nm. Patagium skin (non-ornamental skin under the wing) also reflects in the UV, but epidermis removal on this bare part tended to reduce UV reflectance, whereas removal of the red epidermis of combs increased UV reflectance. Males in better condition (greater body mass relative to size) had bigger and redder combs, but with less UV. Thus, carotenoid pigments of grouse combs are deposited on a white background with significant UV reflectance, which can influence how the signal is perceived by conspecifics. Carotenoid-based traits exhibit UV reflectance in a number of species, but how UV reflectance and carotenoid pigmentation influence colour remains little known for integumentary ornaments compared to plumage traits. UV vision is not uncommon in birds and other animals, so future studies should investigate how UV reflectance influences the perception of carotenoid-based signals of quality.


Carotenoid Colour Red grouse Lagopus lagopus scoticus Sexual selection Ultraviolet vision 



We are grateful to the owner and gamekeepers from the Edinglassie estate for allowing us to collect the data on red grouse. Particular thanks are due to D. Calder for his help with the data collection and to R. Moss for providing specimens of black grouse, capercaillie, and ptarmigan for comb reflectance measurements. We are very grateful to I. Garcia and J. J. Negro (Molecular Ecology Laboratory of Doñana Biological Station, CSIC Spain) for conducting the HPLC analyses on red grouse combs. We also thank M. D. Padilla for transporting samples and C. Alonso-Alvarez for helpful comments on the manuscript. F. Mougeot was supported by a Ramon y Cajal grant (Ministerio de Educación y Ciencia, Spain). L. Pérez-Rodríguez was supported by a pre-doctoral FPU grant (Ministerio de Educación y Ciencia). J. Martínez-Padilla was supported by a post-doctoral grant (ref. EX-27-04-04, Ministerio de Educación y Ciencia). G. Bortolotti was supported by a NSERC grant.


  1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  2. Aust O, Stahl W, Sies H, Tronnier H, Heinrich U (2005) Supplementation with tomato-based products increases lycopene, phytofluene, and phytoene levels in human serum and protects against UV-light-induced erythema. Int J Vitam Nutr Res 75:54–60PubMedCrossRefGoogle Scholar
  3. Badyaev AV, Hill GE (2000) Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol J Linn Soc 69:153–172CrossRefGoogle Scholar
  4. Banks AN (2001) For your eyes only? The role of UV in mate choice. Trends Ecol Evol 16:473–474CrossRefGoogle Scholar
  5. Bart J, Earnst SL (1999) Relative importance of male and territory quality in pairing success of male rock ptarmigan (Lagopus mutus). Behav Ecol Sociobiol 45:355–359CrossRefGoogle Scholar
  6. Bennett ATD, Cuthill IC, Partridge JC, Maier EJ (1996) Ultraviolet vision and mate choice in zebra finches. Nature 380:433–435CrossRefGoogle Scholar
  7. Bleiweiss R (2004) Novel chromatic and structural biomarkers of diet in carotenoid-bearing plumage. Proc R Soc Lond B 271:2327–2335CrossRefGoogle Scholar
  8. Bleiweiss R (2005) Variation in ultraviolet reflectance by carotenoid-bearing feathers of tanagers (Thraupini: Emberizinae: Passeriformes). Biol J Linn Soc 84:243–257CrossRefGoogle Scholar
  9. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127PubMedCrossRefGoogle Scholar
  10. Bortolotti GR (2006) Natural selection and avian coloration: protection, concealment, advertisement or deception? In: Hill GE, McGraw KJ (eds) Avian coloration, vol 2: function and evolution. University Press, Harvard, pp 3–35Google Scholar
  11. Bortolotti GR, Negro JJ, Tella JL, Marchant TA, Bird DM (1996) Sexual dichromatism in birds independent of diet, parasites and androgens. Proc R Soc Lond B 263:1171–1176CrossRefGoogle Scholar
  12. Bortolotti GR, Kimberley JF, Smiths JE (2003) Carotenoid concentration and coloration of American kestrels (Falco sparverius) disrupted by experimental exposure to PCBs. Funct Ecology 17:651–657CrossRefGoogle Scholar
  13. Brawner WR, Hill GE, Sundermann CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid- based plumage pigmentation in male house finches. Auk 117:952–963CrossRefGoogle Scholar
  14. Bright A, Waas JR (2002) Effects of bill pigmentation and UV reflectance during territory establishment in blackbirds. Anim Behav 64:207–213CrossRefGoogle Scholar
  15. Buchholz R (1997) Male dominance and variation in fleshy head ornamentation in wild turkeys. J Avian Biol 28:223–230Google Scholar
  16. Burkhardt D (1989) UV vision: a bird’s eye view of feathers. J Comp Physiol A 164:787–796CrossRefGoogle Scholar
  17. Burley N, Price DK, Zann RA (1992) Bill color, reproduction and condition effects in wild and domesticated zebra Finches. Auk 109:13–23Google Scholar
  18. Cramp S, Simmons KEL (1980) The birds of the western Palearctic, vol 2. Oxford University Press, OxfordGoogle Scholar
  19. Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214CrossRefGoogle Scholar
  20. Darlington RB, Smulders TV (2001) Problems with residual analysis. Anim Behav 62:599–602CrossRefGoogle Scholar
  21. Delahay RJ, Speakman JR, Moss R (1995) The energetic consequences of parasitism—Effects of a developing infection of Trichostrongylus tenuis (Nematoda) on red grouse (Lagopus lagopus scoticus): energy balance, body weight and condition. Parasitology 110:473–482CrossRefGoogle Scholar
  22. Dresp B, Jouventin P, Langley K (2005) Ultraviolet reflecting photonic microstructures in the king penguin beak. Biol Lett 1:310–313PubMedCrossRefGoogle Scholar
  23. Egeland ES, Parker H, Liaaenjensen S (1993) Carotenoids in combs of capercaillie (Tetrao urogallus) fed defined diets. Poultry Sci 72:747–751Google Scholar
  24. Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352Google Scholar
  25. Faivre B, Gregoire A, Preault M, Cezilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103PubMedCrossRefGoogle Scholar
  26. García-Berthou E (2001) On the misuse of residuals in ecology: testing regression residuals vs. The analysis of covariance. J Anim Ecol 70:708–711CrossRefGoogle Scholar
  27. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387PubMedCrossRefGoogle Scholar
  28. Hausmann F, Arnold KE, Marshall NJ, Owens IPF (2003) Ultraviolet signals in birds are special. Proc R Soc Lond B 270:61–67CrossRefGoogle Scholar
  29. Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. J Avian Biol 31:559–566CrossRefGoogle Scholar
  30. Hill GE (2002) A red bird in a brown bag: the function and evolution of ornamental plumage coloration in the house finch. Oxford University Press, OxfordGoogle Scholar
  31. 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
  32. Hill GE, Inouye CY, Montgomerie R (2002) Dietary carotenoids predict plumage coloration in wild house finches. Proc R Soc Lond B 269:1119–1124CrossRefGoogle Scholar
  33. Hollett KG, Thomas VG, MacDonald SD (1984) Structural and functional aspects of supraorbital combs of grouse. In: Hudson P, Lovel TWI (eds) Third International Grouse Symposium. World Pheasant Association, York, pp 193–211Google Scholar
  34. Hudson PJ (1986) The red grouse: the biology and management of a wild gamebird. The Game Conservancy Trust, FordingbridgeGoogle Scholar
  35. Hunt S, Cuthill IC, Bennett ATD, Griffiths R (1999) Preferences for ultraviolet partners in the blue tit. Anim Behav 58:809–815PubMedCrossRefGoogle Scholar
  36. Hunt S, Cuthill IC, Bennett ATD, Church SC, Partridge JC (2001) Is the ultraviolet waveband a special communication channel in avian mate choice? J Exp Biol 204:2499–2507PubMedGoogle Scholar
  37. Hunt S, Kilner RM, Langmore NE, Bennett ATD (2003) Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proc R Soc Lond B 270:S25–S28CrossRefGoogle Scholar
  38. Johnsen A, Andersson S, Ornborg J, Lifjeld JT (1998) Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment. Proc R Soc Lond B 265:1313–1318CrossRefGoogle Scholar
  39. Johnsgard PA (1983) The grouse of the world. Croom Helm, Beckenham, UKGoogle Scholar
  40. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  41. McGraw KJ, Hudon J, Hill GE, Parker RS (2005a) A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behav Ecol Sociobiol 57:391–397CrossRefGoogle Scholar
  42. McGraw KJ, Hill GE, Parker RS (2005b) The physiological costs of being colourful: nutritional control of carotenoid utilization in the American goldfinch, Carduelis tristis. Anim Behav 69:653–660CrossRefGoogle Scholar
  43. McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122CrossRefGoogle Scholar
  44. Mínguez-Mosquera I (1993) Clorofilas y carotenoides en tecnologia de alimentos. Universidad de Sevilla, Sevilla, SpainGoogle Scholar
  45. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: Indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159Google Scholar
  46. Moss R (1972) Food selection by red grouse (Lagopus lagopus scoticus (Lath.)) in relation to chemical composition. J Anim Ecol 41:411–423CrossRefGoogle Scholar
  47. Mougeot F, Arroyo BE (2006) Ultraviolet reflectance by the cere of raptors. Biol Lett 2:173–176PubMedCrossRefGoogle Scholar
  48. Mougeot F, Redpath S (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433CrossRefGoogle Scholar
  49. Mougeot F, Irvine J, Seivwright LJ, Redpath S, Piertney SB (2004) Testosterone, immunocompetence and honest sexual signaling in male red grouse. Behav Ecol 15:630–637CrossRefGoogle Scholar
  50. Mougeot F, Redpath SM, Leckie F (2005a) Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus: sexual ornaments reflects nematode parasite intensity. J Avian Biol 36:203–209CrossRefGoogle Scholar
  51. Mougeot F, Dawson A, Redpath S, Leckie F (2005b) Testosterone and autumn territorial behaviour in male red grouse Lagopus lagopus scoticus. Horm Behav 47:576–584PubMedCrossRefGoogle Scholar
  52. Mougeot F, Evans S, Redpath S (2005c) Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour in male red grouse. Oecologia 144:289–298PubMedCrossRefGoogle Scholar
  53. Mougeot F, Redpath S, Piertney SB, Hudson PJ (2005d) Separating behavioural and physiological mechanisms in testosterone mediated trade-offs. Am Nat 166:158–168PubMedCrossRefGoogle Scholar
  54. Mundinger PC (1972) Annual testicular cycle and bill color change in the eastern American goldfinch. Auk 89:403–419Google Scholar
  55. Negro JJ, Figuerola J, Garrido J, Green AJ (2001) Fat stores in birds: an overlooked sink for carotenoid pigments? Funct Ecol 15:297–303CrossRefGoogle Scholar
  56. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  57. Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in Birds—Implications for new theories of sexual selection. Trends Ecol Evol 10:44–47CrossRefGoogle Scholar
  58. Peters A, Denk AG, Delhey AG, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120PubMedCrossRefGoogle Scholar
  59. Redpath S, Mougeot F, Leckie F, Evans S (2006) The effects of autumn testosterone on survival and productivity in red grouse Lagopus lagopus scoticus. Anim Behav 71:1297–1305CrossRefGoogle Scholar
  60. Rintamaki PT, Hoglund J, Karvonen E, Alatalo RV, Bjorklund N, Lundberg A, Ratti O, Vouti J (2000) Combs and sexual selection in black grouse (Tetrao tetrix). Behav Ecol 11:465–471CrossRefGoogle Scholar
  61. SAS (2001) SAS/STAT user’s guide, version 8.01. SAS Institute, Cary, NCGoogle Scholar
  62. Seivwright LJ, Redpath S, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78:69–76PubMedCrossRefGoogle Scholar
  63. Seivwright LJ, Redpath S, Mougeot F, Leckie F, Hudson PJ (2005) Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse. Proc R Soc Lond B 272:1299–1304CrossRefGoogle Scholar
  64. Shawkey MD, Hill GE (2005) Carotenoids need structural colours to shine. Biol Lett 1:12–124CrossRefGoogle Scholar
  65. Siitari H, Viitala J (2002) Behavioural evidence for ultraviolet vision in a tetraonid species: foraging experiment with black grouse Tetrao tetrix. J Avian Biol 33:199–202CrossRefGoogle Scholar
  66. Stahl W, Sies H (2002) Carotenoids and protection against solar UV radiation. Skin Pharmacol Appl Skin Physiol 15:291–296PubMedCrossRefGoogle Scholar
  67. Thompson CW, Hillgarth N, Leu M, McClure HE (1997) High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am Nat 149:270–294CrossRefGoogle Scholar
  68. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266:1–12CrossRefGoogle Scholar
  69. Wynn-Williams DD, Edwards HGM (2002) Environmental UV radiation: biological strategies for protection and avoidance. In: Horneck G, Baumstark-Khan C (eds) Astrobiology. The quest for the conditions of life. Springer, Berlin Heidelberg New York, pp 245–260Google Scholar
  70. Zuk M, Johnsen TS, Maclarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond B 260:205–210CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • F. Mougeot
    • 1
    • 2
    • 3
  • J. Martínez-Padilla
    • 2
  • L. Pérez-Rodríguez
    • 1
  • G. R. Bortolotti
    • 4
  1. 1.Instituto de Investigación en Recursos Cinegéticos (IREC, CSIC-UCLM-JCCM)Ciudad RealSpain
  2. 2.Centre for Ecology and Hydrology, BanchoryBanchoryUK
  3. 3.School of Biological SciencesUniversity of AberdeenAberdeenUK
  4. 4.University of SaskatchewanSaskatoonCanada

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