Skip to main content
SpringerLink
Log in

Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

The possible integration of different sexual ornaments into a composite system, and especially the information content of such ornament complexes, is poorly investigated. Many bird species display complex plumage coloration, but whether this represents one integrated or several independent sexual traits can be unclear. Collared flycatchers (Ficedula albicollis) display melanised and depigmented plumage areas, and the spectral features (brightness and UV chroma) of these are correlated with each other across the plumage. In a 5-year dataset of male and female plumage reflectance, we examined some of the potential information content of integrated, plumage-level colour attributes by estimating their relationships to previous and current year body condition, laying date and clutch size. Females were in better condition the year before they became darker pigmented, and males in better current year condition were also darker pigmented. Female pigment-based brightness was positively, while male structurally based brightness was negatively related to current laying date. Finally, the overall UV chroma of white plumage areas in males was positively associated with current clutch size. Our results show that higher degree of pigmentation is related to better condition, while the structural colour component is associated with some aspects of reproductive investment. These results highlight the possibility that correlated aspects of a multiple plumage ornamentation system may reflect together some aspects of individual quality, thereby functioning as a composite signal.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Almasi B, Roulin A, Korner-Nievergelt F, Jenni-Eiermann S, Jenni L (2012) Coloration signals the ability to cope with elevated stress hormones: effects of corticosterone on growth of barn owls are associated with melanism. J Evol Biol 25:1189–1199

    Article  PubMed  CAS  Google Scholar 

  • Andersson (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Bonser RHC (1995) Melanin and the abrasion resistance of feathers. Condor 97:590–591

    Article  Google Scholar 

  • Cornwallis CK, Uller T (2010) Towards an evolutionary ecology of sexual traits. Trends Ecol Evol 25:145–152

    Google Scholar 

  • Cramp S, Perrins CM, Brooks DJ (1993) The birds of the Western Palearctic, Volume 7: Old World flycatchers to shrikes. Oxford University Press, Oxford

    Google Scholar 

  • Daan S, Dijkstra C, Tinbergen JM (1990) Family planning in the kestrel (Falco tinnunculus): the ultimate control of laying date and clutch size. Behaviour 114:83–116

    Article  Google Scholar 

  • Doucet SM, Mennill DJ, Montgomerie R, Boag PT, Ratcliffe LM (2004) Achromatic plumage reflectance predicts reproductive success in male black-capped chickadees. Behav Ecol 16:218–222

    Article  Google Scholar 

  • Duckworth RA, Badyaev AV, Parlow AF (2003) Elaborately ornamented males avoid costly parental care in the house finch (Carpodacus mexicanus): a proximate perspective. Behav Ecol Sociobiol 55:176–183

    Article  Google Scholar 

  • Ducrest A-L, Keller L, Roulin R (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510

    Article  PubMed  Google Scholar 

  • Evans SR, Sheldon BC (2012) Quantitative genetics of a carotenoid-based color: Hheritability and persistent natal environmental effects in the Great Tit. Am Nat 179:79–94

    Article  PubMed  Google Scholar 

  • Fitze PS, Richner H (2002) Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol 13:401–407

    Article  Google Scholar 

  • Galván I (2010) Plumage coloration can be perceived as a multiple condition-dependent signal by Great Tits Parus major. Ibis 152:359–367

    Article  Google Scholar 

  • Galván I (2011) Feather microstructure predicts size and colour intensity of a melanin-based plumage signal. J Avian Biol 42:473–479

    Article  Google Scholar 

  • Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS ONE 10:e3335

    Article  Google Scholar 

  • Griffith SG (2000) A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus. Proc R Soc Lond B 267:1115–1119

    Article  CAS  Google Scholar 

  • Griffith SC, Owens IPF, Burke T (1999) Environmental determination of a sexually selected trait. Nature 400:358–360

    Article  CAS  Google Scholar 

  • Griggio M, Serra L, Licheri D, Campomori C, Pilastro A (2009) Moult speed affects structural feather ornaments in the blue tit. J Evol Biol 22:782–792

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson L, Qvarnström A, Sheldon BC (1995) Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313

    Article  CAS  Google Scholar 

  • Hanssen SA, Folstad I, Erikstad KE (2006) White plumage reflects individual quality in female eiders. Anim Behav 71:337–343

    Article  Google Scholar 

  • Hargitai R, Török J, Tóth L, Hegyi G, Rosivall B, Szigeti B, Szöllősi E (2005) Effects of environmental conditions and parental quality on inter- and intraclutch egg-size variation in the Collared Flycatcher (Ficedula albicollis). Auk 122:509–522

    Article  Google Scholar 

  • Harshman LG, Zera JA (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86

    Article  PubMed  Google Scholar 

  • Hasson O (1990) Amplifiers and their role in the evolution of male display. Evol Ecol 4:277–289

    Article  Google Scholar 

  • Hasson O (1991) Sexual displays as amplifiers: practical examples with an emphasis on feather decorations. Behav Ecol 2:189–197

    Article  Google Scholar 

  • Hegyi G, Garamszegi LZ, Eens M, Török J (2008a) Female ornamentation and territorial conflicts in collared flycatchers (Ficedula albicollis). Naturwissenschaften 95:993–996

    Article  PubMed  CAS  Google Scholar 

  • Hegyi G, Rosivall B, Szöllősi E, Hargitai R, Eens M, Török J (2007a) A role for female ornamentation in the facultatively polygynous mating system of collared flycatchers. Behav Ecol 18:1116–1122

    Article  Google Scholar 

  • Hegyi G, Rosivall B, Szöllősi E, Hargitai R, Eens M, Török J (2008b) Phenotypic plasticity in a conspicuous female plumage trait: information content and mating patterns. Anim Behav 75:977–989

    Article  Google Scholar 

  • Hegyi G, Szigeti B, Török J, Eens M (2007b) Melanin, carotenoid and structural plumage ornaments: information content and role in great tits. J Avian Biol 38:698–708

    Article  Google Scholar 

  • Hegyi G, Szöllősi E, Jenni-Eiermann S, Török J, Eens M, Garamszegi LZ (2010) Nutritional correlates and mate acquisition role of multiple sexual traits in male collared flycatchers. Naturwissenschaften 97:567–576

    Article  PubMed  CAS  Google Scholar 

  • Hegyi G, Török J, Garamszegi LZ, Rosivall B, Szöllősi E, Hargitai R (2007c) Dynamics of multiple sexual signals in relation to climatic conditions. Evol Ecol Res 9:905–920

    Google Scholar 

  • Hegyi G, Török J, Tóth L, Garamszegi LZ, Rosivall B (2006) Rapid temporal change in the expression and age-related information content of a sexually selected trait. J Evol Biol 19:228–238

    Article  PubMed  CAS  Google Scholar 

  • Hill GE, Brawner WR III (1998) Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proc R Soc Lond B 265:1105–1109

    Article  Google Scholar 

  • Hill GE, McGraw KJ (eds) (2006) Bird coloration. Harvard University Press, Cambridge

    Google Scholar 

  • Hoi H, Griggio M (2008) Dual utility of a melanin-based ornament in bearded tits. Ethology 114:1094–1100

    Article  Google Scholar 

  • Horváthová T, Nakagawa S, Uller T (2012) Strategic female reproductive investment in response to male attractiveness in birds. Proc R Soc Lond B 279:163–170

    Article  Google Scholar 

  • Höglund J, Sheldon BC (1998) The cost of reproduction and sexual selection. Oikos 83:478–483

    Article  Google Scholar 

  • Jawor JM, Gray N, Beall SM, Breitwisch R (2004) Multiple ornaments correlate with aspects of condition and behaviour in female northern cardinals, Cardinalis cardinalis. Anim Behav 67:875–882

    Article  Google Scholar 

  • Kemp DJ, Vukusic P, Rutowski RL (2006) Stress-mediated covariance between nano-structural architecture and ultraviolet butterfly coloration. Funct Ecol 20:282–289

    Article  Google Scholar 

  • Kullberg C, Houston DC, Metcalfe NB (2002) Impaired flight ability – a cost of reproduction in female blue tits. Behav Ecol 13:575–579

    Article  Google Scholar 

  • Laczi M, Török J, Rosivall B, Hegyi G (2011) Integration of spectral reflectance across the plumage: implications for mating patterns. PLoS ONE 6:e23201

    Article  PubMed  CAS  Google Scholar 

  • Matrková J, Remeš V (2012) Environmental and genetic effects on pigment-based vs. structural component of yellow feather colouration. PLoS ONE 7:e36640

    Article  PubMed  Google Scholar 

  • McGlothlin JW, Duffy DL, Henry-Freeman JL, Ketterson ED (2007) Diet quality affects an attractive white plumage pattern in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 61:1391–1399

    Article  Google Scholar 

  • McGraw KJ (2006) Dietary mineral content influences the expression of melanin-based ornamental coloration. Behav Ecol 18:137–142

    Article  Google Scholar 

  • McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:1525–1531

    Article  CAS  Google Scholar 

  • McGraw KJ, Mackillop EA, Dale J, Hauber ME (2002) Different colours reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J Exp Biol 205:3747–3755

    PubMed  Google Scholar 

  • Michl G, Török J, Griffith S, Sheldon BC (2002) Experimental analysis of sperm competition mechanisms in a wild bird population. Proc Natl Acad Sci USA 99:5466–5470

    Article  PubMed  CAS  Google Scholar 

  • Michl G, Török J, Péczely P, Garamszegi LZ, Schwabl H (2005) Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behav Ecol 16:383–388

    Article  Google Scholar 

  • Niecke M, Rothlaender S, Roulin A (2003) Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers. Oecologia 137:153–158

    Article  PubMed  Google Scholar 

  • Pärt T, Qvarnström A (1997) Badge size in collared flycatchers predicts outcome of mate competition over territories. Anim Behav 54:893–899

    Article  Google Scholar 

  • Piault R, Gasparini J, Bize P, Jenni-Eiermann S, Roulin A (2009) Pheomelanin-based coloration and the ability to cope with variation in food supply and parasitism. Am Nat 174:548–556

    Article  PubMed  Google Scholar 

  • Piault R, van den Brink V, Roulin A (2012) Condition-dependent expression of melanin-based coloration in the Eurasian kestrel. Naturwissenschaften 99:391–396

    Article  PubMed  CAS  Google Scholar 

  • Prum RO (2006) Anatomy, physics, and evolution of structural colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 1, 1st edn. Harvard University Press, Harvard, pp 295–353

    Google Scholar 

  • Quesada J, Senar JC (2009) Cross-fostering experiments to compare carotenoid- and melanin-based plumage traits and long-term parental effects in post-moulted great tits. Behaviour 146:1235–1251

    Article  Google Scholar 

  • Roulin A (2004) Proximate basis of the covariation between a melanin-based female ornament and offspring quality. Oecologia 140:668–675

    Article  PubMed  Google Scholar 

  • Roulin A, Almasi B, Meichtry-Stier KS, Jenni L (2011) Eumelanin- and pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. J Evol Biol 24:2241–2247

    Article  PubMed  CAS  Google Scholar 

  • Roulin A, Almasi B, Rossi-Pedruzzi A, Ducrest AL, Wakamatsu K, Miksik I, Blount JD, Jenni-Eiermann S, Jenni L (2008) Corticosterone mediates the condition-dependent component of melanin-based coloration. Anim Behav 75:1351–1358

    Article  Google Scholar 

  • Roulin A, Dijkstra C (2003) Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90:359–364

    Article  PubMed  CAS  Google Scholar 

  • Roulin A, Ducrest A-L (2013) Genetics of colouration in birds. Semin Cell Dev Biol 24:594–608

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Romano M, Rubolini D, Teplitsky C, Ambrosini R, Caprioli M, Canova L, Wakamatsu K (2013) Sexual dimorphism in melanin pigmentation, feather coloration and its heritability in the barn swallow (Hirundo rustica). PLoS ONE 8:e58024

    Article  PubMed  CAS  Google Scholar 

  • Senar JC, Camerino M, Copete JL, Metcalfe NB (1993) Variation in black bib of the Eurasian siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110:924–927

    Article  Google Scholar 

  • Senar JC, Figuerola J, Domènech J (2003) Plumage coloration and nutritional condition in the great tit (Parus major): the roles of carotenoids and melanins differ. Naturwissenschaften 90:234–237

    PubMed  CAS  Google Scholar 

  • Serra L, Griggio M, Licheri D, Pilastro A (2007) Moult speed constrains the expression of a carotenoid-based sexual ornament. J Evol Biol 20:2028–2034

    Article  PubMed  CAS  Google Scholar 

  • Shawkey MD, Estes AM, Siefferman L, Hill GE (2003) Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour. Proc R Soc Lond B 270:1455–1460

    Article  Google Scholar 

  • Shawkey MD, Estes AM, Siefferman L, Hill GE (2005) The anatomical basis of sexual dichromatism in non-iridescent ultraviolet-blue structural coloration of feathers. Biol J Linn Soc 84:259–271

    Article  Google Scholar 

  • Siefferman L, Hill GE (2003) Structural and melanin coloration indicate parental effort and reproductive success in male eastern bluebirds. Behav Ecol 14:855–861

    Article  Google Scholar 

  • Siefferman L, Hill GE (2005a) Evidence for sexual selection on structural plumage coloration in female eastern bluebirds (Sialia sialis). Evolution 59:1819–1828

    PubMed  Google Scholar 

  • Siefferman L, Hill GE (2005b) Male eastern bluebirds trade future ornamentation for current reproductive investment. Biol Lett 1:208–211

    Article  PubMed  Google Scholar 

  • Siitari H, Huhta E (2002) Individual color variation and male quality in pied flycatchers (Ficedula hypoleuca): a role of ultraviolet reflectance. Behav Ecol 13:737–741

    Article  Google Scholar 

  • Slagsvold T, Lifjeld JT (1992) Plumage color is a condition-dependent sexual trait in male pied flycatchers. Evolution 46:825–828

    Article  Google Scholar 

  • Stjernman M, Råberg L, Nilsson J (2004) Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites? Proc R Soc Lond B 271:2387–2394

    Article  Google Scholar 

  • Svensson L (1992) Identification guide to European passerines. Märstatryck, Stockholm

    Google Scholar 

  • Török J, Hargitai R, Hegyi G, Matus Z, Michl G, Péczely P, Rosivall B, Tóth G (2007) Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order. Behav Ecol Sociobiol 61:541–550

    Article  Google Scholar 

  • Török J, Hegyi G, Garamszegi LZ (2003) Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav Ecol 14:382–388

    Article  Google Scholar 

  • Török J, Hegyi G, Tóth L, Könczey R (2004) Unpredictable food supply modifies costs of reproduction and hampers individual optimization. Oecologia 141:432–443

    Article  PubMed  Google Scholar 

  • Veiga JP, Puerta M (1996) Nutritional constraints determine the expression of a sexual trait in the house sparrow, Passer domesticus. Proc R Soc Lond B 263:229–234

    Article  Google Scholar 

  • Vergara P, Fargallo JA, Martínez-Padilla J, Lemus JA (2009) Inter-annual variation and information content of melanin-based coloration in female Eurasian kestrels. Biol J Linn Soc 97:781–790

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to A. Roulin and anonymous reviewers for comments on the manuscript. We wish to thank G. Blázi, R. Főző, L.Z. Garamszegi, E. Szász and A. Szegedi for help with the fieldwork. This research was funded by a Bolyai fellowship to G.H., OTKA grants PD72117 and K101611 to G.H., PD75481 and F68295 to B.R. and K75618 to J.T., the Eötvös Loránd University (PhD scholarship) to M.L., the Erdők a Közjóért Alapítvány and the Pilis Park Forestry. During all stages of this work, G.M. was supported by TÁMOP-4.2.1./B-09/1-KMR-2010-0005 and TÁMOP-4.2.2./B-10/1-2010-0023. This research was conducted in agreement with the current laws of Hungary.

Author information

Authors and Affiliations

  1. Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, Pázmány Péter Sétány 1/C, 1117, Budapest, Hungary

    Miklós Laczi, Gergely Hegyi, Márton Herényi, Dorottya Kiss, Gábor Markó, Gergely Nagy, Balázs Rosivall, Eszter Szöllősi & János Török

  2. Department of Plant Pathology, Corvinus University of Budapest, Ménesi út 44, 1118, Budapest, Hungary

    Gábor Markó

Authors
  1. Miklós Laczi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gergely Hegyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Márton Herényi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dorottya Kiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gábor Markó
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gergely Nagy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Balázs Rosivall
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eszter Szöllősi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. János Török
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miklós Laczi.

Additional information

Communicated by: Alexandre Roulin

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laczi, M., Hegyi, G., Herényi, M. et al. Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher. Naturwissenschaften 100, 983–991 (2013). https://doi.org/10.1007/s00114-013-1099-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-013-1099-1

Keywords

Search

Navigation