Skip to main content
Log in

Specific immunity and polymorphism of breeding plumage in pied flycatcher (Ficedula hypoleuca) males (Aves: Passeriformes)

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The relationship between the type of melanin-based plumage colouration and the strength of experimentally induced immune response was studied using as an example a pied flycatcher population from the Moscow region. The breeding plumage of pied flycatcher males exhibits the full spectrum of transitions from contrasting black-and-white to cryptic brownish, the latter being very similar to the colouration of females. In spite of numerous studies, the nature of this polymorphism still remains vague. Unlike many other avian species with monocyclic breeding, a considerable fraction of pied flycatchers overlaps two energy-consuming productive processes, breeding and moult, over the whole species range. During the main experimental treatment we activated the humoral immunity of free-living males in chick-rearing period by injection of nonpathogenic multifactorial antigen (sheep red blood cells, SRBC) and estimated the strength of the immune responses after repeated captures in 6–8 days. In addition, after each capture we evaluated the numbers of leucocytes (WBC), heterophil to lymphocyte ratios (H/L) and measured night time basal metabolic rates (BMR). Non-moulting males of different colour types showed the same immune responses. Among moulting birds, the strength of the immune response was significantly higher in pale males (morphs 4–7 by Drost’s scale) than in bright males with rich melanin-based colouration (morphs 2–3). This difference resulted from two opposite processes. During moulting, pale males heightened the antibody titer after immunization, while bright males tended to reduce the strength of immune response. Possibly such an asymmetry in immunocompetence at the first stage of moult reflects the different life strategies of pied flycatcher males—conspicuous birds less commonly overlap breeding with moult than cryptic ones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Artzy-Randrup, Y. and Kondrashov, A.S., Sympatric speciation under incompatibility selection, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 31, pp. 11619–11624.

    Article  PubMed  CAS  Google Scholar 

  • Bushuev, A.V., Kerimov, A.B., and Ivankina, E.V., Estimation of heritability and repeatability of resting metabolic rate in birds, with free-living Pied Flycatchers Ficedula hypoleuca (Aves: Passeriformes) as an example, Zh. Obshch. Biol., 2010, vol. 71, no. 5, pp. 403–425.

    Google Scholar 

  • Dale, S. and Slagsvold, T., Mate choice on multiple cues, decision rules and sampling strategies in female pied flycatchers, Behaviour, 1996, vol. 133, nos. 11/12, pp. 903–944.

    Article  Google Scholar 

  • Dein, J., Hematology, in Clinical Avian Medicine, Harrison, G.J., and Harrison, W.R., Eds., London: Saunders, 1986, pp. 174–191.

    Google Scholar 

  • Dolnik, V.R. and Gavrilov, V.M., Bioenergetics of molt in the chaffinch (Fringilla coelebs), Auk, 1979, vol. 96, no. 2, pp. 253–264.

    Google Scholar 

  • Drost, R., Über das Brutkleid männlicher Trauerfliegenfänger, Muscicapa hypoleuca, Vogelzug, 1936, vol. 6, pp. 179–186.

    Google Scholar 

  • Ducrest, A.-L., Keller, L., and Roulin, A., Pleiotropy in the melanocortin system, coloration and behavioural syndromes, Trends Ecol. Evol., 2008, vol. 23, no. 9, pp. 502–510.

    Article  PubMed  Google Scholar 

  • Fargallo, J.A., Padilla, J.M., Díaz, A.D., Moreno, J.S., and Dávila, J.A., Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels, J. Anim. Ecol., 2007, vol. 76, no. 1, pp. 201–209.

    Article  PubMed  Google Scholar 

  • Fitze, P.S. and Richner, H., Differential effects of a parasite on ornamental structures based on melanins and carotenoids, Behav. Ecol., 2002, vol. 13, no. 3, pp. 401–407.

    Article  Google Scholar 

  • Fitze, P.S., Tschirren, B., Gasparini, J., and Richner, H., Carotenoid-based plumage colors and immune function: is there a trade-off for rare carotenoids?, Am. Nat., 2007, vol. 169, suppl. 1, pp. 137–144.

    Article  Google Scholar 

  • Gasparini, J., Bize, P., Piault, R., Wakamatsu, K., Blount, J.D., Ducrest, A.-L., and Roulin, A., Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls, J. Anim. Ecol., 2009, vol. 78, no. 3, pp. 608–616.

    Article  PubMed  Google Scholar 

  • Gavrilov, V.M., Kerimov, A.B., and Ivankina, E.V., Population and geographic variation of plumage color and metabolism in males of different color type in The Pied Flycatcher Ficedula hypoleuca, Dokl. Akad. Nauk, 1993, vol. 333, no. 6, pp. 807–810.

    Google Scholar 

  • Gavrilov, V.M., Kerimov, A.B., Golubeva, T.B., Ivankina, E.V., and Ilyina, T.A., Ecological energetics and population ecology of the great tit, in Kol’tsevanie v izuchenii migratsii ptits v Rossii i sopredel’nykh gosudarstvakh. 1986–1987 gg. (Banding in the Study of Bird Migration in Russia and Neighboring Countries: 1986–1987), Moscow: Nauka, 1994, pp. 110–158.

    Google Scholar 

  • Gonzalez, G., Sorci, G., and de Lope, F., Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus), Behav. Ecol. Sociobiol., 1999, vol. 46, no. 2, pp. 117–122.

    Article  Google Scholar 

  • Górecki, A., Kalabukhov-Skvortsov respirometer and resting metabolic rate measurement, in IBP Handbook no. 24: Methods for Ecological Energetics, Grodzin-ski, W., Klekowski, R.Z., and Duncan, A., Eds., Oxford, UK: Blackwell, 1975, pp. 309–313.

    Google Scholar 

  • Griffith, S.C., Parker, T.H., and Olson, V.A., Melaninversus carotenoid-based sexual signals: is the difference really so black and red?, Anim. Behav., 2006, vol. 71, no. 4, pp. 749–763.

    Article  Google Scholar 

  • Gross, W.B. and Siegel, H.S., Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens, Avian Dis., 1983, vol. 27, no. 4, pp. 972–979.

    Article  PubMed  CAS  Google Scholar 

  • Hamilton, W.D. and Zuk, M., Heritable true fitness and bright birds: a role for parasites?, Science, 1982, vol. 218, no. 4570, pp. 384–387.

    Article  PubMed  CAS  Google Scholar 

  • Harris, J. and Bird, D.J., Supernatants from leucocytes treated with melanin-concentrating hormone (MCH) and α-melanocyte stimulating hormone (α-MSH) have a stimulatory effect on rainbow trout (Oncorhynchus mykiss) head kidney phagocytes in vitro, Vet. Immunol. Immunopathol., 2000, vol. 76, nos. 1/2, pp. 117–124.

    Article  PubMed  CAS  Google Scholar 

  • Hill, R.W., Determination of oxygen consumption by use of the paramagnetic oxygen analyzer, J. Appl. Physiol., 1972, vol. 33, no. 2, pp. 261–263.

    PubMed  CAS  Google Scholar 

  • Hõrak, P., Ots, I., and Murumägi, A., Hematological health state indices of reproducing great tits: a response to brood size manipulation, Funct. Ecol., 1998, vol. 12, no. 5, pp. 750–756.

    Article  Google Scholar 

  • Horak, P., Surai, P.F., Ots, I., and Møller, A.P., Fat soluble antioxidants in brood-rearing great tits Parus major: relations to health and appearance, J. Avian Biol., 2004, vol. 35, no. 1, pp. 63–70.

    Article  Google Scholar 

  • Hõrak, P., Sild, E., Soomets, U., Sepp, T., and Kilk, K., Oxidative stress and information content of black and yellow plumage coloration: an experiment with greenfinches, J. Exp. Biol., 2010, vol. 213, no. 13, pp. 2225 2233.

    Article  PubMed  Google Scholar 

  • Houde, A.E. and Torio, A.J., Effect of parasitic infection on male color pattern and female choice in guppies, Behav. Ecol., 1992, vol. 3, no. 4, pp. 346–351.

    Article  Google Scholar 

  • Ivankina, E.V., Ilyina, T.A., and Kerimov, A.B., The male plumage variability and the strategy of attracting a female: the estimation of the advertising behaviour’s spatial organisation in bright and cryptically coloured Pied Flycatcher males (Ficedula hypoleuca, Passeriformes, Aves), Zh. Obshch. Biol., 1995, vol. 56, no. 6, pp. 762–775.

    Google Scholar 

  • Ivankina, E.V., Kerimov, A.B., Grinkov, V.G., and Bushuev, A.V., Structural and functional aspects of variation of ornamentation of breeding plumage in pied fly-catcher (Ficedula hypoleuca) males (Aves: Passeriformes), Zh. Obshch. Biol., 2007, vol. 68, no. 4, pp. 278–295.

    PubMed  CAS  Google Scholar 

  • Jacquin, L., Lenouvel, P., Haussy, C., Ducatez, S., and Gasparini, J., Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia, J. Avian Biol., 2011, vol. 42, no. 1, pp. 11–15.

    Article  Google Scholar 

  • Järvi, T., Røskaft, E., Bakken, M., and Zumsteg, B., Evolution of variation in male secondary sexual characteristics: a test of eight hypotheses applied to pied flycatchers, Behav. Ecol. Sociobiol., 1987, vol. 20, no. 3, pp. 161–169.

    Article  Google Scholar 

  • Kerimov, A.B. and Ivankina, E.V., The basal metabolic rate and its relationship to social and reproductive status in individual passerine birds, in Proc. 22th Int. Ornithol. Congr. Durban, Adams, N.J. and Slotow, R.H., Eds., Johannesburg: BirdLife South Africa, 1999a, pp. 370–389.

    Google Scholar 

  • Kerimov, A.B. and Ivankina, E.V., The relations between resting metabolic rate of fledglings and father’s colour type in the pied flycatcher (Ficedula hypoleuca), The Ring, 1999b, vol. 21, no. 1, p. 203.

    Google Scholar 

  • Kerimov, A.B., Ivankina, E.V., Ilyina, T.A., and Bushuev, A.V., Energy heterogeneity of a polymorphic population of the pied flycatcher Ficedula hypoleuca in the breeding season, in Populyatsionnaya ekologiya zhivotnykh (Animal Population Ecology), Moskvitina, N.S., Ed., Tomsk: Tomsk. Gos. Univ., 2006, pp. 35–36.

    Google Scholar 

  • Lampe, H.M. and Espmark, Y.O., Song structure reflects male quality in pied flycatcher, Ficedula hypoleuca, Anim. Behav., 1994, vol. 34, no. 4, pp. 869–876.

    Article  Google Scholar 

  • Lawler, E.M. and Redig, P.T., The antibody responses to sheep red blood cells of the red-tailed hawk and great-horned owl, Dev. Comp. Immunol., 1984, vol. 8, no. 3, pp. 733–738.

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, A. and Alatalo, R.V., The Pied Flycatcher, London: T. and A.D. Poyser, 1992.

    Google Scholar 

  • Männiste, M. and Hörak, P., Effects of immune activation and glucocorticoid administration on feather growth in greenfinches, J. Exp. Zool., 2011, vol. 315, no. 9, pp. 527–535.

    Article  Google Scholar 

  • Martin II, L.B., Scheuerlein, A., and Wikelski, M., Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs?, Proc. Royal Soc. London: B, 2002, vol. 270, no. 1511, pp. 153–158.

    Article  Google Scholar 

  • Martin II, L.B., Trade-offs between molt and immune activity in two populations of house sparrows (Passer domesticus), Can. J. Zool., 2005, vol. 83, no. 6, pp. 780–787.

    Article  Google Scholar 

  • Maxwell, M.H., Avian blood leucocyte responses to stress, Worlds Poult. Sci. J., 1993, vol. 49, no. 1, pp. 34–43.

    Article  Google Scholar 

  • Maynard Smith, J. and Harper, D.G.C., The evolution of aggression: can selection generate variability?, Phil. Trans. Royal Soc. London: B, 1988, vol. 319, no. 1196, pp. 557–570.

    Article  CAS  Google Scholar 

  • McGraw, K.J., The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants?, Anim. Behav., 2005, vol. 69, no. 4, pp. 757–764.

    Article  Google Scholar 

  • Moreno-Rueda, G., Experimental test of a trade-off between moult and immune response in house sparrows Passer domesticus, J. Evol. Biol., 2010, vol. 23, no. 10, pp. 2229–2237.

    Article  PubMed  CAS  Google Scholar 

  • Moreno, J. and Møller, A.P., Are melanin ornaments signals of antioxidant and immune capacity in birds?, Acta Zool. Sin., 2006, vol. 52, no. 1, pp. 202–228.

    CAS  Google Scholar 

  • Moreno, J., Sanz, J.J., Merino, S., and Arriero, E., Daily energy expenditure and cell-mediated immunity in pied flycatchers while feeding nestlings: interaction with moult, Oecologia, 2001, vol. 129, no. 4, pp. 492–497.

    Google Scholar 

  • Moreno, J., Velando, A., Ruiz-de-Castañeda, R., Cantarero, A., Gonzáles-Braojos, S., and Redondo, A., Plasma antioxidant capacity and oxidative damage in relation to male plumage ornamental traits in a montane Iberian pied flycatcher Ficedula hypoleuca population, Acta Ornithologica, 2011, vol. 46, no. 1, pp. 65–70.

    Article  Google Scholar 

  • Moshkin, M.P., Gerlinskaya, L.A., and Evsikov, V.I., The role of the immune system in behavioral strategies of reproduction, J. Reprod. Devel., 2000, vol. 46, no. 6, pp. 341–365.

    Article  CAS  Google Scholar 

  • Mougeot, F., Galván, I., and Alonso-Alvarez, C., Contrasted effects of an oxidative challenge and α-melanocyte-stimulating hormone on cellular immune responsiveness: an experiment with red-legged partridges Alectoris rufa, Oecologia, 2012, vol. 169, no. 2, pp. 385–394.

    Article  PubMed  Google Scholar 

  • Nava, M.P., Veiga, J.P., and Puerta, M., White blood cell counts in house sparrows (Passer domesticus) before and after moult and after testosterone treatment, Can. J. Zool., 2001, vol. 79, no. 1, pp. 145–148.

    CAS  Google Scholar 

  • Olson, V.A. and Owens, I.P.F., Costly sexual signals: are carotenoids rare, risky or required?, Trends Ecol. Evol., 1998, vol. 13, no. 12, pp. 510–514.

    Article  PubMed  CAS  Google Scholar 

  • Ots, I., Kerimov, A.B., Ivankina, E.V., Ilyina, T.A., and Hörak, P., Immune challenge affects basal metabolic activity in wintering great tits, Proc. Royal Soc. London: B, 2001, vol. 268, no. 1472, pp. 1175–1181.

    Article  CAS  Google Scholar 

  • Saks, L., Ots, I., and Hörak, P., Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence, Oecologia, 2003, vol. 134, no. 3, pp. 301–307.

    PubMed  Google Scholar 

  • Sanz, J.J., Moreno, J., Merino, S., and Tomás, G., Trade-off between two resource-demanding functions: post-nuptial moult and immunity during reproduction in male pied flycatchers, J. Anim. Ecol., 2004, vol. 73, no. 3, pp. 441–447.

    Article  Google Scholar 

  • Schmidt-Nielsen, K., Animal Physiology: Adaptation and Environment, 4th ed., Cambridge: Cambridge Univ. Press, 1980.

    Google Scholar 

  • Silverin, B., Fänge, R., Viebke, P.-A., and Westin, J., Seasonal changes in mass and histology of the spleen in willow tits Parus montanus, J. Avian Biol., 1999, vol. 30, no. 3, pp. 255–262.

    Article  Google Scholar 

  • Slagsvold, T. and Lifjeld, J.T., Plumage colour is a condition-dependent sexual trait in male pied flycatchers, Evolution, 1992, vol. 46, no. 3, pp. 825–828.

    Article  Google Scholar 

  • Sætre, G.-P., Fossnes, T., and Slagsvold, T., Food provisioning in the pied flycatcher: do females gain direct benefits from choosing bright-coloured males?, J. Anim. Ecol., 1995, vol. 64, no. 1, pp. 21–30.

    Article  Google Scholar 

  • Vysotsky, V.G., Determination of the age of pied flycatchers (Ficedula hypoleuca) during the breeding season, Tr. Zool. Inst. Akad. Nauk SSSR, 1989, vol. 197, pp. 49–52.

    Google Scholar 

  • Walther, B.A., Clayton, D.H., and Gregory, R.D., Showiness of Neotropical birds in relation to ectoparasite abundance and foraging stratum, Oikos, 1999, vol. 87, no. 1, pp. 157–165.

    Article  Google Scholar 

  • Wegmann, T.G. and Smithies, O., A simple hemagglutination system requiring small amounts of red cells and antibodies, Transfusion, 1966, vol. 6, no. 1, pp. 67–73.

    Article  Google Scholar 

  • Wilson, J.D., A re-assessment of the significance of status singnalling in populations of wild great tits, Parus major, Anim. Behav., 1992, vol. 43, no. 6, pp. 999–1009.

    Article  Google Scholar 

  • Zuk, M., Parasites and bright birds: new data and a new prediction, in Bird-Parasite Interactions: Ecology, Evolution, and Behaviour, Loye, J.E. and Zuk, M., Eds., Oxford, UK: Oxford Univ. Press, 1991, pp. 317–327.

    Google Scholar 

  • Zuk, M., Thornhill, R., Ligon, J.D., and Johnson, K., Parasites and mate choice in red jungle fowl, Am. Zool., 1990, vol. 30, no. 2, pp. 235–244.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. B. Kerimov.

Additional information

Published in Russian in Zhurnal Obshchei Biologii, 2012, Vol. 73, No. 5, pp. 349–359.

The article was translated by the authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kerimov, A.B., Rogovin, K.A., Ivankina, E.V. et al. Specific immunity and polymorphism of breeding plumage in pied flycatcher (Ficedula hypoleuca) males (Aves: Passeriformes). Biol Bull Rev 3, 232–240 (2013). https://doi.org/10.1134/S2079086413030067

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086413030067

Keywords

Navigation