Naturwissenschaften

, Volume 97, Issue 7, pp 637–644 | Cite as

Detrimental effects of carotenoid pigments: the dark side of bright coloration

  • Kristal A. Huggins
  • Kristen J. Navara
  • Mary T. Mendonça
  • Geoffrey E. Hill
Original Paper

Abstract

Carotenoid pigments produce yellow, orange, and red integumentary color displays that can serve as reliable signals of health and condition. In many birds and fish, individuals gain competitive or mating advantages by ingesting and utilizing large quantities of carotenoid pigments. Carotenoid pigments serve as antioxidants, performing important functions as free-radical scavengers. The beneficial effects of carotenoid pigments are well documented, but rarely have researchers considered potential detrimental effects of high-level accumulation of carotenoids. We maintained American goldfinches (Carduelis tristis) on high- or low-carotenoid diets through molt and tested for damage to the liver and skeletal muscle. High intake of carotenoids had no measurable effect on liver enzymes but caused an increase in creatine kinase, an indicator of skeletal muscle breakdown, and a reduction in vertical flight performance, a measure of skeletal muscle integrity. The detrimental effects of high-level carotenoid accumulation were approximately equivalent to the negative effects of removing carotenoids from the diet. The adverse effects observed in this study have important implications for theories of the function and evolution of colorful plumage.

Keywords

Carduelis tristis Honest signaling Lutein Muscle breakdown Sexual selection 

Notes

Acknowledgements

Birds were collected and handled according to federal (# 21661), state (#97181), and IACUC (2005-0825) permits. We thank Erin Carroll, Tyler Hicks, and Maranda B. Wood-Holley for assistance with collecting and husbandry and Bob Montgomerie for use of his software for calculating yellow chroma. Work was funded by NSF grants IBN0235778 and DEB0218313 to G.E.H.

References

  1. Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration. Vol 1. Measurements and mechanisms. Harvard Univesity Press, Cambridge, MassachusettesGoogle Scholar
  2. Askew GN, Marsh RL (2002) Muscle designed for maximum short-term power output: quail flight muscle. J Exp Biol 205:2153–2160PubMedGoogle Scholar
  3. Blomhoff R (2001) Vitamin A and carotenoid toxicity. Food Nutr Bull 22:320–334Google Scholar
  4. Bollinger T, Wobeser G, Clark RG, Nieman DJ, Smith JR (1989) Concentration of creatine kinase and aspartate aminotransferase in the blood of wild mallards following capture by three methods for banding. J Wildl Dis 25:225–231PubMedGoogle Scholar
  5. Brawner WR, Hill GE, Sunderman CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male house finches. Auk 117:952–963CrossRefGoogle Scholar
  6. Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370CrossRefGoogle Scholar
  7. Dial KP, Biewener AA (1993) Pectoralis force and power output during different modes of flight in pigeons (Columba livia). J Exp Biol 176:31–54Google Scholar
  8. Gaal T, Mezes M, Noble RC, Dixon J, Speake BK (1995) Development of antioxidant capacity in tissues of the chick embryo. Comp Biochem Physiol B 112:711–716CrossRefGoogle Scholar
  9. Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322CrossRefGoogle Scholar
  10. Guglielmo CG, Peirsma T, Williams TD (2001) A sport-physiological perspective on bird migration: evidence for flight-induced muscle damage. J Exp Biol 204:2683–2690PubMedGoogle Scholar
  11. Harr KR (2002) Clinical chemistry of companion avian species: a review. Vet Clin Pathol 31:140–151CrossRefPubMedGoogle Scholar
  12. Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? TREE 19:353–354PubMedGoogle Scholar
  13. Hartman FA (1961) Locomotor mechanisms in birds. Smithson Misc Collect 143:1–99Google Scholar
  14. Hathcock JN, Hattan DG, Jenkins MY, McDonald JT, Sundaresan PR, Wilkening VL (1990) Evaluation of vitamin A toxicity. Am J Clin Nutr 52:183–202PubMedGoogle Scholar
  15. Hill GE (1995) Seasonal variation in circulating carotenoid pigments in the house finch. Auk 112:1057–1061Google Scholar
  16. Hill GE (2002) A red bird in a brown bag: the function and evolution of ornamental carotenoid plumage coloration in the house finch. Oxford University Press, New YorkGoogle Scholar
  17. Hill GE (2006) Environmental regulation of ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, Volume 1: mechanisms and measurements. Harvard University Press, CambridgeGoogle Scholar
  18. Hill GE (2007) Melanins and carotenoids as feather colorants and signals. In: Jamieson BGM (ed) Reproductive biology and phylogeny of birds, vol 6B. Science Publishers, EnfieldGoogle Scholar
  19. Hill GE, Farmer KL (2005) Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92:30–34CrossRefPubMedGoogle Scholar
  20. Hill GE, Farmer KL, Beck ML (2004) The effect of micoplasmosis on carotenoid plumage coloration in male house finches. J Exp Biol 207:2095–2099CrossRefPubMedGoogle Scholar
  21. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton, NJGoogle Scholar
  22. Jaensch SM, Cullen L, Raidal SR (2000) Assessment of liver function in galahs (Eolophus roseicapillus) after partial hepatectomy: a comparison of plasma enzyme concentrations, serum bile acid levels, and galactose clearance tests. Avian Medicine and Surgery 14:164–171CrossRefGoogle Scholar
  23. Jakubowski J, Aebischer V, Luetzelschwab J, Vogel B, Donatsch P, Cordier A (1998) Stability of CK and LDH-isoenzymes values in minipig serum under different storage conditions. Scand J Lab Anim Sci Suppl 25:205–209Google Scholar
  24. Lanzarot MP, Barahona MV, San Andrés MI, Fernández-García M, Rodríguez C (2005) Hematologic, protein electrophoresis, biochemistry, and cholinesterase values of free-living black stork nestlings (Cicona nigra). J Wildl Dis 41:379–386PubMedGoogle Scholar
  25. Lawson NS, Haven GT, Williams GW (1982) Analyte stability in clinical chemistry quality control materials. Crit Rev Clin Lab Sci 17:1–50CrossRefPubMedGoogle Scholar
  26. Lindstrom K, Lundstrom J (2000) Male greenfinches (Carduelis chloris) with brighter ornaments have higher virus infection clearance rates. Behav Ecol Sociobiol 48:44–51CrossRefGoogle Scholar
  27. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311CrossRefGoogle Scholar
  28. MacDougall AK, Montgomerie R (2003) Assortative mating by carotenoid-based plumage color: a quality indicator in American goldfinches, Carduelis tristis. Naturwissenschaften 90:464–467CrossRefPubMedGoogle Scholar
  29. Martin HD, Ruck C, Schmidt M, Sell S, Beutner S, Mayer B, Walsh R (1999) Chemistry of carotenoid oxidation and free radical reactions. Pure Applied Chemistry 71:2253–2262CrossRefGoogle Scholar
  30. McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, volume 1: measurements and mechanisms. Harvard University Press, CambridgeGoogle Scholar
  31. McGraw KJ, Gregory AJ (2004) Carotenoid pigments in male American goldfinches: what is the optimal strategy for becoming colorful? Biol J Linn Soc 83:273–280CrossRefGoogle Scholar
  32. McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:1525–1531CrossRefGoogle Scholar
  33. McGraw KJ, Hill GE (2001) Carotenoid access and intraspecific variation in plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Cardinalis cardinalis). Funct Ecol 15:732–739CrossRefGoogle Scholar
  34. McGraw KJ, Hill GE, Stradi R, Parker RS (2002) The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch. Comp Biochem Physiol, B 131:261–269CrossRefGoogle Scholar
  35. McGraw KJ, Hill GE, Navara KJ, Parker RS (2004) Differential accumulation and pigmenting ability of dietary carotenoids in colorful finches. Physiol Biochem Zool 77:484–491CrossRefPubMedGoogle Scholar
  36. McGraw KJ, Hill GE, Parker RS (2005) The physiological costs of being colorful: nutritional control of carotenoid utilization in the American goldfinch (Carduelis tristis). Anim Behav 69:653–660CrossRefGoogle Scholar
  37. Mitchell MA, Sandercock DA (1995) Creatine kinase isoenzyme profiles in the plasma of the domestic fowl (Gallus domesticus): effects of acute heat stress. Res Vet Sci 59:30–34CrossRefPubMedGoogle Scholar
  38. Navara KJ, Hill GE (2003) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916CrossRefGoogle Scholar
  39. Negro J, Brotolotti GR, Tella JL, Fernie KJ, Bird DM (1998) Regulation of integumentary colour and plasma carotenoids in American kestrels consistent with sexual selection theory. Funct Ecol 12:307–312CrossRefGoogle Scholar
  40. O'Connell MJ, Powell P, Brennan D, Lynch T, McCarthy CJ, Eustace SJ (2002) Whole body MR imaging in the diagnosis of polymyositis. Am J Roentgenol 179:967–971Google Scholar
  41. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky, or required. Trends Ecol Evol 13:510–515CrossRefGoogle Scholar
  42. Palozza P (1998) Prooxidant actions of carotenoids in biological systems. Nutr Rev 56:257–265PubMedCrossRefGoogle Scholar
  43. Palozza P, Calviello G, Bartoli GM (1995) Prooxidant activity of β-carotene under 100% oxygen pressure in rat liver microsomes. Free Radic Biol Med 19:887–892CrossRefPubMedGoogle Scholar
  44. Russel RM (1999) The vitamin A spectrum: from deficiency to toxicity. Am J Clin Nutr 71:878–884Google Scholar
  45. Saks L, McGraw KJ, Horak P (2003) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561CrossRefGoogle Scholar
  46. Schmitz HH, Poor CL, Wellman RB, Erdman JW (1991) Concentrations of selected carotenoids and vitamin A in human liver, kidney, and lung tissue. J Nutr 121:1613–1621PubMedGoogle Scholar
  47. 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 colouration. Proc R Soc Lond Series B 273:2985–2991CrossRefGoogle Scholar
  48. Sibley DA (2000) The Sibley guide to birds. Chanticleer Press, New YorkGoogle Scholar
  49. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, New YorkGoogle Scholar
  50. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham, UKGoogle Scholar
  51. Veasey JS, Metcalfe NB, Houston DC (1998) A reassessment of the effect of body mass upon flight speed and predation risk in birds. Anim Behav 56:883–889CrossRefPubMedGoogle Scholar
  52. Volfinger L, Lassourd V, Michaus JM, Braun JP, Toutain P (1994) Kinetic evaluation of muscle damage during exercise by calculation of the amount of creatine kinase released. Am J Physiol 266:R434–R441PubMedGoogle Scholar
  53. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzel H (1999) Good genes, oxidative stress, and condition-dependent signals. Proc R Soc Lond B 266:1–12CrossRefGoogle Scholar
  54. Zahavi A, Zahavi A (1997) The handicap principle: a missing piece of Darwin's puzzle. Oxford University Press, OxfordGoogle Scholar
  55. Zhao W, Han Y, Zhao B, Hirota A, Hou J, Xin W (1998) Effect of carotenoids on respiratory burst of rat peritoneal macrophages. Biochim Biophys Acta 1381:77–88PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Kristal A. Huggins
    • 1
  • Kristen J. Navara
    • 2
  • Mary T. Mendonça
    • 1
  • Geoffrey E. Hill
    • 1
  1. 1.Department of Biological SciencesAuburn UniversityAuburnUSA
  2. 2.Department of Poultry ScienceUniversity of GeorgiaAthensUSA

Personalised recommendations