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Oecologia

, Volume 134, Issue 3, pp 301–307 | Cite as

Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence

  • Lauri Saks
  • Indrek Ots
  • Peeter Hõrak
Ecophysiology

Abstract

Hypotheses of parasite-mediated sexual selection (PMSS) propose that elaborate male ornaments have evolved due to female preferences. Females would benefit from mating with more ornamented males if males' ornamentation signals their health status and ability to provide parasite resistance genes for the offspring. Carotenoid-based plumage coloration of birds has been hypothesised to honestly reflect an individual's health status due to trade-off in allocation of carotenoids between maintenance and signalling functions. The prediction of this hypothesis, namely that individuals with brighter plumage are able to mount stronger immune responses against novel antigens and reveal generally better health state, was tested in captive male greenfinches (Carduelis chloris). Greenfinches with brighter yellow breast feathers showed stronger humoral immune response against novel antigen (SRBC) while no relationship between plumage coloration and an estimate of cell-mediated immune responsiveness (PHA response) was detected. Elaborately ornamented individuals had better general health state as indicated by the negative correlations between plumage brightness and heterophil haemoconcentration. Consistent with the concept of PMSS, these results suggest that carotenoid-based plumage coloration in greenfinches honestly signals immunocompetence and health status.

Keywords

Carduelis chloris Carotenoids Immune response Leukocytes Plumage colour 

Notes

Acknowledgements

We thank the staff of Kabli Ornithological Station (especially Agu Leivits) for providing facilities and assistance in trapping birds. We are grateful to Karin Lindström who inspected the blood samples for Sindbis virus antibodies and Helen Vellau for counting leukocytes. We thank Ulvi Karu, Lea Tegelmann, Ene Sarapuu and Helen Vellau for assistance in taking care of the birds and for data collection, and Jan Lunström for valuable advice about keeping the greenfinches in captivity. Two anonymous referees provided constructive criticism of the manuscript. The study was financially supported by Estonian Science Foundation grant no. 4537 (to P.H.).

References

  1. Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Can J Zool 79:101–105CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, N.J.Google Scholar
  3. Apanius V (1998) Stress and immune defence. In: Møller AP, Milinski M, Slater PBJ (eds) Advances in the study of behaviour,27. Academic Press, San Diego, pp 133–153Google Scholar
  4. Birkhead TR, Flecher F, Pellatt EJ (1998) Sexual selection in the zebra finch (Taeniopygia guttata): condition, sex traits and immune capacity. Behav EcolSociobiol 44:179–191CrossRefGoogle Scholar
  5. Boa-Amponsem K, Larsen CT, Dunnington EA, Price SEH, Yang A, Siegel PB (1998) Mode of inheritance of unselected traits in lines of chickens selected for high or low antibody response tp sheep red blood cells. 1. Resistance to marble spleen disease virus and juvenile body weight. Poultry Sci 77:1073–1080Google Scholar
  6. Boa-Amponsem K, Price SEH, Dunnington EA, Siegel PB (2001) Effect of route of inoculation on humoral immune response of white leghorn chickens selected for high or low antibody response to sheep red blood cells. Poultry Sci 80:1073–1078Google Scholar
  7. 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 Ser B 263:1171–1176Google Scholar
  8. Burley N, Tidemann SC, Halupka K (1991) Bill colour and parasite levels of zebra finches. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution and behaviour. Oxford University Press, Oxford, pp 359–375Google Scholar
  9. Camplani A, Saino N, Møller AP (1999) Carotenoids, sexual signals and immune function in barn swallows from Chernobyl. Proc R Soc Lond Ser B 266:1111–1116CrossRefGoogle Scholar
  10. Clayton DH (1991) The influence of parasites on host sexual selection. Parasitol Today 7:329–340Google Scholar
  11. Cramp P, Perrins CM (eds) (1994) The birds of the western Palearctic,Vol 7. Oxford University Press, OxfordGoogle Scholar
  12. Darwin C (1871) The descent of man and selection in relation to sex. Murray, LondonGoogle Scholar
  13. Dein J (1986) Hematology. In: Harrison GJ, Harrison WR (eds) Clinical avian medicine. Saunders, London, pp 178–191Google Scholar
  14. Dufva R, Allander K (1995) Intraspecific variation in plumage coloration reflects immune response in great tit (Parus major) males. Funct Ecol 9:785–789Google Scholar
  15. Dunnington EA, Siegel PB (1984) Age and body weight at sexual maturity in female white leghorn chickens. Poultry Sci 63:828–830Google Scholar
  16. Eley C (1991) Status signalling in the western greenfinch(Carduelis chloris). PhD thesis, University of Sussex, Brighton, UKGoogle Scholar
  17. Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J LinnSoc 41:315–352Google Scholar
  18. Fox DL (1979) Biochromy. University of California Press, Berkeley, Calif.Google Scholar
  19. Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohaemagglutinin skin response in thymectomized chickens. Poultry Sci 52:246–250Google Scholar
  20. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546PubMedGoogle Scholar
  21. Gray DA (1996) Carotenoids and sexual dichromatism in North American passerine birds. Am Nat 148:453–480CrossRefGoogle Scholar
  22. Grether FG, Hudon J, Millie DF (1999) Carotenoid limitation of sexual selection along an environmental gradient in guppies. Proc R Soc Lond Ser B 266:1317–1322CrossRefGoogle Scholar
  23. Grill CP, Rush VN (2000) Analysing spectral data: comparison and application of two techniques. Biol J Linn Soc 69:121–138CrossRefGoogle Scholar
  24. Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972–979PubMedGoogle Scholar
  25. Gross WG, Siegel HS, Hall RW, Domermuth CH, Du Rose RT (1980) Production and persistence of antibodies in chickens to sheep erythrocytes. 2. Resistance to infectious diseases. Poultry Sci 59:205–210Google Scholar
  26. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedGoogle Scholar
  27. Hamilton WJ, Poulin R (1997) The Hamilton-Zuk hypothesis revised: a meta-analytical approach. Behaviour 134:299–320Google Scholar
  28. Harmon BG (1998) Avian heterophils in inflammation and disease resistance. Poultry Sci 77:972–977Google Scholar
  29. Hill GE (1992) Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109:1–12Google Scholar
  30. Hill GE, Montgomerie R, Inouye C, Dale J (1994) Influence of dietary carotenoids on plasma and plumage colour in the house finch: intra- and intersexual variation. Funct Ecol 8:64–73Google Scholar
  31. Hõrak P, Saks L, Ots I, Kollist H (2002) Repeatability of condition indices in captive greenfinches (Carduelis chloris). Can J Zool 80:636–643CrossRefGoogle Scholar
  32. Korpimäki E, Tolonen P, Bennett GF (1995) Blood parasites, sexual selection and reproductive success of European kestrels. Ecoscience 2:335–343Google Scholar
  33. Lawler EM, Redig PT (1984) The antibody responses to sheep red blood cells of the red-tailed hawk and great-horned owl. Dev Comp Immunol 8:733–738PubMedGoogle Scholar
  34. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121Google Scholar
  35. Lifjeld JI, Dunn PI, Whittingham LI (2002) Short-term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130:185–190Google Scholar
  36. Lindström K, Lundsrtöm J (2000) Male greenfinches (Carduelis chloris) with brighter ornaments have higher virus infection clearance rate. Behav Ecol Sociobiol 48:44–51CrossRefGoogle Scholar
  37. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311Google Scholar
  38. Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci USA 98:2071–2076CrossRefPubMedGoogle Scholar
  39. Maxwell MH (1993) Avian blood leukocyte response to stress. World Poultry Sci J 49:34–43Google Scholar
  40. Merilä J, Sheldon BC (1999) Testis size variation in the greenfinch (Carduelis chloris): relevance for some recent models of sexual selection. Behav Ecol Sociobiol 45:115–123CrossRefGoogle Scholar
  41. Merilä J, Sheldon BC, Lindström K (1999) Plumage brightness in relation to hematozoan infections in the greenfinch (Carduelis chloris): bright males are a good bet. Ecoscience 6, 12–18.Google Scholar
  42. Moore CB, Siopes TD (2000) Effects of lighting conditions and melatonin supplementation on the cellular and humoral immune responses in Japanese quail, (Coturnix coturnix japonica). Gen Comp Endocrinol 119:95–104CrossRefPubMedGoogle Scholar
  43. Møller AP (1991) Sperm competition, sperm depletion, paternal care and relative testis size in birds. Am Nat 110:275–297Google Scholar
  44. Møller AP (1998) Evidence of larger impact of parasites on host in the tropics: investment in immune function within and outside the tropics. Oikos 82:265–270Google Scholar
  45. Møller AP, Petrie M (2002) Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol 13:248–253CrossRefGoogle Scholar
  46. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176Google Scholar
  47. Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20.PubMedGoogle Scholar
  48. 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 Poultry Sci Rev 11:137–159Google Scholar
  49. Munns PL, Lamont SJ (1991) Effects of age and immunisation interval on the anamnestic response to T-cell-dependent and T-cell-independent antigens in chickens. Poultry Sci 70:2371–2374Google Scholar
  50. Nunn CL, Gittleman JL, Antonovics J (2000) Promiscuity and the primate immune system. Science 290:1168–1170PubMedGoogle Scholar
  51. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  52. Ots I, Murumägi A, Hõrak P (1998) Haematological health state indicates of reproducing great tits: methodology and sources of variation. Funct Ecol 12:700–707CrossRefGoogle Scholar
  53. Parmentier HK, Nieuwland MGB, Rijke E, Schrama JW (1996) Divergent antibody responses to vaccines and divergent body weights of chicken lines selected for high and low humoral responsiveness to sheep red blood cells. Avian Dis 40:634–644PubMedGoogle Scholar
  54. Preault M (1999) Stratégie d'appariement et selection sexuelle chez le merle noir, (Turdus merula), en milieu urbain. MSc thesis, Université de Bourgongne, Dion, FranceGoogle Scholar
  55. Rice WR, Gaines SD (1994) "Heads I win, tails you lose": testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol Evol 9:235–237Google Scholar
  56. Roulin A, Jungi TW, Pfister H, Dijkstra C (2000) Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond Ser B 267:937–941CrossRefGoogle Scholar
  57. Saino N, Ninni P, Calza S, De Bernardi F, Møller AP (2000) Better red than dead: carotenoid-based gape coloration reveals health status in barn swallow nestlings. Proc R Soc Lond Ser B 267:57–61CrossRefGoogle Scholar
  58. Schulz JH, Bermudez AJ, Tomlinson JL, Firman JD, He ZQ (1998) Effects of implanted radiotransmitters on captive mourning doves. J Wildl Manage 62:1451–1460Google Scholar
  59. Seutin G (1994) Plumage redness in redpoll finches does not reflect hemoparasitic infection. Oikos 70:280–286Google Scholar
  60. Siegel PB, Gross WB (1980) Production and persistence of antibodies in chickens to sheep erythrocytes. 1. Directional selection. Poultry Sci 59:1–5Google Scholar
  61. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  62. Stradi R, Celentano G, Rossi E, Rovati G, Pastore M (1995) Carotenoids in bird plumage. I. The carotenoid pattern in a series of Palearctic carduelinae. Comp Biochem Physiol B Biochem Mol Biol110:131–143Google Scholar
  63. Svensson L (1992) Identification guide to European passerine birds. Svenssson, StockholmGoogle Scholar
  64. Totzke U, Fenske M, Hüppop O, Raabe H, Schach N (1999) The influence of fasting on blood and plasma composition of herring gulls (Larus argentatus). Physiol Biochem Zool 72:426–437CrossRefPubMedGoogle Scholar
  65. Trust KA, Fairbrother A, Hooper MJ (1994) Effects of 7,12-dimethylbenz[a]anthracene on immune function and mixed-function oxygenase activity in the European starling. Environ Toxicol Chem 13:821–830Google Scholar
  66. Verhulst S, Dieleman SJ, Parmentier HK (1999) A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc Natl Acad Sci USA 96:4478–4481CrossRefPubMedGoogle Scholar
  67. Weatherhead PJ, Merz KJ, Bennet GF, Irwin RE (1993) Parasites faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav Ecol Sociobiol 75:13–23Google Scholar
  68. Wegmann TG, Smithies O (1966) A simple haemagglutination system requiring small amount of red cells and antibodies. Transfusion 6:67–73Google Scholar
  69. Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53: 205–214PubMedGoogle Scholar
  70. Zuk M, Johnsen TS (1998) Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc R Soc Lond Ser B 265:1631–1635CrossRefGoogle Scholar
  71. Zuk M, Johnsen TS, MacLarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond Ser B 260:205–210Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Institute of Zoology and HydrobiologyTartu UniversityTartu Estonia

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