Advertisement

Journal of Comparative Physiology B

, Volume 181, Issue 2, pp 269–275 | Cite as

Fat stores in a migratory bird: a reservoir of carotenoid pigments for times of need?

  • Benjamin J. MetzgerEmail author
  • Franz Bairlein
Original Paper

Abstract

Carotenoids are well known for their immune-stimulant function in birds and other vertebrates. Moreover, they have potential antioxidant capacity, scavenging free radicals and protecting cell compartments from oxidation. Most essential carotenoids are fat soluble and could be stored for times of need especially in adipose tissues, built up by migratory birds as the main source of energy on long-distance flights. In an exclusive diet experiment, garden warblers (Sylvia borin) were fed ad libitum with an experimental diet, enriched with two different dose rates of carotenoids, or with control food, during the period of their first autumn migration. Plasma carotenoid content was measured via HPLC and chroma of plasma and fat examined with a spectrophotometer. Birds were infected with Isospora spp. and intensity of infection determined by oocyst counts 3 days post infection. Plasma lutein levels and chroma of subcutaneous fat stores were positively correlated and chroma values of these fat stores increased in the birds that got the higher dose rate, whereas they decreased significantly in the control group after infection with Isospora spp. Chroma of subcutaneous fat deposits in vivo and intensity of Isospora infection were negatively correlated. By measuring the chroma of fat deposits in vivo, we show that fat can be a reservoir for carotenoids. These colorful antioxidants are stored in the fat and taken from there in times of a higher demand, e.g. when mounting an immune response to parasites.

Keywords

Chroma Garden warbler Immune challenge Isospora Lutein Subcutaneous fat deposits 

Notes

Acknowledgments

We are grateful to U. Strauß and A. Völk for help with bird maintenance. T. Klinner, U. Pianovska and J. Delingat helped with lab work. P. H. Becker and R. Nagel provided logistical support. O. Dolnik gave critical comments especially concerning parasitological aspects. The work benefited from remarks of two anonymous referees. All birds were taken from the wild and held under license of Ministry of Environment of Lower Saxony, Germany. All experiments were conducted under licence of Weser-Ems District Government, Lower Saxony, Germany (no. 509f-42502-32/12). The work was funded by the German Science Foundation (DFG).

References

  1. Allen PC, Fetterer RH (2002) Interaction of dietary vitamin E with Eimeria maxima infections in chickens. Poult Sci 81:41–48PubMedGoogle Scholar
  2. Bairlein F (1986) Ein standardisiertes Futter für Ernährungsuntersuchungen an omnivoren Kleinvögeln. J Ornithol 127:338–340CrossRefGoogle Scholar
  3. Bairlein F (1990) Nutrition and food selection in migratory birds. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 198–213Google Scholar
  4. Bairlein F (1991) Sylvia borin (Boddaert 1783)—Gartengrasmücke. In: Glutz von Blotzheim UN, Bauer KM (eds) Handbuch der Vögel Mitteleur. Aula, Wiesbaden, pp 888–889Google Scholar
  5. Bairlein F (1996) Fruit-eating in birds and its nutritional consequences. Comp Biochem Physiol 113:215–224CrossRefGoogle Scholar
  6. Bairlein F (2002) How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds (rev). Naturwissenschaften 89:1–10CrossRefPubMedGoogle Scholar
  7. Bairlein F, Gwinner E (1994) Nutritional mechanisms and temporal control of migratory energy accumulation in birds. Annu Rev Nutr 14:187–215CrossRefPubMedGoogle Scholar
  8. Bairlein F, Totzke U (1992) New aspects on migratory physiology of trans-Saharan passerine migrants. Ornis Scand 23:244–250CrossRefGoogle Scholar
  9. Castaneda MP, Hirschler EM, Sams AR (2005) Skin pigmentation evaluation in broilers fed natural and synthetic pigments. Poult Sci 84:143–147PubMedGoogle Scholar
  10. Chew BP (1993) Role of carotenoids in the immune response. J Dairy Sci 76:2804–2811CrossRefPubMedGoogle Scholar
  11. Constantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds? Funct Ecol 22:367–370CrossRefGoogle Scholar
  12. Costantini D, Dell’Omo G (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol 145:137–142CrossRefGoogle Scholar
  13. Costantini D, Cardinale M, Carere C (2007) Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp Biochem Physiol 144:363–371Google Scholar
  14. Costantini D, Dell’Ariccia G, Lipp HP (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211:377–381CrossRefPubMedGoogle Scholar
  15. Di Mascio P, Murphy ME, Sies H (1991) Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols. Am J Clin Nutr 53:194–200Google Scholar
  16. Dolnik OV (2002) Some aspects of the biology and host-parasite interactions of Isospora spp. (Protozoa: Coccidiida) of passerine birds. Dissertation, University of OldenburgGoogle Scholar
  17. Dolnik OV (2006) The relative stability of chronic Isospora sylvianthina (Protozoa: Apicomplexa) infection in blackcaps (Sylvia atricapilla): evaluation of a simplified method of estimating isosporan infection intensity in passerine birds. Parasitol Res 100:155–160CrossRefPubMedGoogle Scholar
  18. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  19. Gray DA (1996) Carotenoids and sexual dichromatism in North American passerine birds. Am Nat 148:453–480CrossRefGoogle Scholar
  20. Gul M, Demircan B, Taysi S, Oztasan N, Gumustekin K, Siktar E, Polat F, Akar S, Akcay F, Dane S (2006) Effects of enduracne training and acute exhaustive exercise on antioxidant defense mechanisms in rat heart. Comp Biochem Physiol 143:239–245CrossRefGoogle Scholar
  21. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387CrossRefPubMedGoogle Scholar
  22. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339CrossRefGoogle Scholar
  23. Hill GE (1995) Interspecific variation in plasma hue in relation to carotenoid plumage pigmentation. Auk 112:1054–1057Google Scholar
  24. Holden JM, Eldridge AL, Beecher GR, Buzzard IM, Bhagwat S, Davi CS, Douglass LW, Gebhardt S, Haytowitz D, Schakel S (1999) Carotenoid content of US foods: an update of the database. J Food Comp Anal 12:169–196CrossRefGoogle Scholar
  25. Horak P, Saks L, Karu U, Ots I, Surai P, McGraw K (2004) How coccidian parasites affect health and appearance of greenfinches. J Anim Ecol 71:935–947CrossRefGoogle Scholar
  26. Ji LL (1999) Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med 222:283–292CrossRefPubMedGoogle Scholar
  27. Kaiser A (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. J Field Ornithol 64:246–255Google Scholar
  28. Kershaw E, Flier J (2004) Adipose tissue as an endocrine organ. J Clin Endocr Metabol 89:2548–2556CrossRefGoogle Scholar
  29. Kowaltowski AJ, Vercesi AE (1999) Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med 26:463–471CrossRefPubMedGoogle Scholar
  30. Krinsky NI (1993) Actions of carotinoids in biological systems. Ann Rev Nutr 13:561–587CrossRefGoogle Scholar
  31. Latscha T (1990) Carotenoids: their nature and significance in animal feeds. Roche, Basel (Publication 2175)Google Scholar
  32. McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration mechanisms and measurements. Harvard University Press, Cambridge, pp 177–242Google Scholar
  33. McGraw KJ, Toomey MB (2010) Carotenoid accumulation in the tissues of zebra finches: predictors of integumentary pigmentation and implications for carotenoid allocation strategies. Physiol Biochem Zool 83:97–109CrossRefPubMedGoogle Scholar
  34. McGraw KJ, Hill GE, Navara KJ, Parker RS (2004) Differential accumulation and pigmentation ability of dietary carotenoids in colorful finches. Physiol Biochem Zool 77:484–491CrossRefPubMedGoogle Scholar
  35. McGraw KJ, Crino OL, Medina-Jerez W, Nolan PM (2006) Effect of dietary carotenoid supplementation on food intake and immune function in a songbird with no carotenoid coloration. Ethology 112:1209–1216CrossRefGoogle Scholar
  36. McGraw KJ, Tourville E, Butler M (2008) A quantitative comparison of the commonly used methods for extracting carotenoids from avian plasma. Behav Ecol Sociobiol 62:1991–2002CrossRefGoogle Scholar
  37. McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393CrossRefGoogle Scholar
  38. Møller AP, de Lope F, Saino N (2004) Parasitism, immunity, and arrival date in a migratory bird, the barn swallow. Ecology 85:206–219CrossRefGoogle Scholar
  39. Nachtigall W (1990) Wind tunnel measurements of long-time flights in relation to the energetics and water economy of migrating birds. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 319–327Google Scholar
  40. Negro JJ, Figuerola J, Garrido J, Green AJ (2001) Fat stores in bird: an overlooked sink for carotenoid pigments? Funct Ecol 15:297–303CrossRefGoogle Scholar
  41. Olson VA, Owens IPF (1999) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  42. Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Horak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175–1181CrossRefGoogle Scholar
  43. Scott I, Evans PR (1992) The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue liver and skeletal muscle: implications for BMR/body mass relationships. Comp Biochem Physiol 103:329–332CrossRefGoogle Scholar
  44. Scott I, Mitchell PI, Evans PR (1996) How does variation body composition affect the basal metabolic rates of birds? Funct Ecol 10:307–313CrossRefGoogle Scholar
  45. Tella JL, Negro JJ, Rodríguez-Estrella R, Blanco G, Forero MG, Blázquez MC, Hiraldo F (1998) A comparison of spectrophotometry and color charts for evaluating total plasma carotenoids in wild birds. Physiol Zool 71:708–711PubMedGoogle Scholar
  46. Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser H (2003) Costs of migration in free-flying songbirds. Nature 423:704CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Institute of Avian Research “Vogelwarte Helgoland”WilhelmshavenGermany

Personalised recommendations