Skip to main content
SpringerLink
Log in

Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

An Erratum to this article was published on 18 May 2010

Abstract

Many colourful sexually selected signals in animals are carotenoid-dependent and, because carotenoids function as antiradicals and immunostimulating molecules, carotenoid-dependent signals may honestly reflect the health state of individuals. Some others nutrients like vitamin A may also enhance health and colouration, but these have rarely been tested alongside carotenoids in colourful birds. Here, we examined whether beak colour of the spotless starling (Sturnus unicolor) reflected circulating levels of carotenoids and/or vitamin A (retinol). Spotless starlings are polygynous, sexually dimorphic birds (i.e. length of chest feathers). The tip of the beaks of male and female spotless starlings is more intensely coloured at the beginning of the breeding season and becomes dull after mating, which may suggest a sexual function. We found that females have a more intensely coloured beak and higher plasma carotenoid concentration than males during mating, and, despite the finding that carotenoid and vitamin A levels were not significantly related; colour intensity was positively correlated with plasma concentration of carotenoids and vitamin A in both sexes. However, adult beak coloration was not associated with carotenoid and vitamin A concentrations after nestlings were hatched. Therefore, beak colouration of spotless starlings provides information about circulating levels of carotenoids and vitamins during the mating season and may potentially function as a reliable signal of physiological status in the context of sexual selection.

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

Similar content being viewed by others

References

  • Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Amundsen T, Pärn H (2006) Female colouration: review of functional and non-functional hypotheses. In: Hill GE, McGraw KJ (eds) Bird coloration. Vol. 2, Function and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • Aparicio JM, Cordero PJ, Veiga JP (2001) A test of the hypothesis of mate choice based on heterozygosity in the spotless starling. Anim Behav 61:1001–1006

    Article  Google Scholar 

  • Avilés JM, Soler JJ, Navarro C, Pérez-Contreras T (2008) Dark nests and nestling conspicuousness in color patterns of altricial birds. Am Nat 171:327–338

    Article  PubMed  Google Scholar 

  • Bertrand S, Faivre B, Sorci G (2006) Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants? J Exp Biol 209:4414–4419

    Article  CAS  PubMed  Google Scholar 

  • Biard C, Surai PF, Møller AP (2007) An analysis of pre- and post-hatching maternal effects mediated by carotenoids in the blue tit. J Evol Biol 20:326–339

    Article  CAS  PubMed  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  CAS  PubMed  Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (1995) Carotenoids. Volume IA: isolation and analysis. Birkhäuser, Basel

    Google Scholar 

  • Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445

    Article  Google Scholar 

  • Burley N, Coopersmith CB (1987) Bill color preferences of zebra finches. Ethology 76:133–151

    Article  Google Scholar 

  • Burley NT, Price DK, Zann RA (1992) Bill color, reproduction and condition effects in wild and domesticated zebra finches. Auk 109:13–23

    Google Scholar 

  • Burton GW, Ingold KU (1984) β-carotene: an unusual type of lipid antioxidant. Science 224:569–573

    Article  CAS  PubMed  Google Scholar 

  • Chastel O, Lacroix A, Weimerskirch H, Gabrielsen GW (2005) Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird. Horm Behav 47:459–466

    Article  CAS  PubMed  Google Scholar 

  • Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S–261S

    CAS  PubMed  Google Scholar 

  • Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370

    Article  Google Scholar 

  • Cramp S (1998) Cramp’s the complete birds of the Western Palearctic. Optimedia. Oxford University Press, Oxford

    Google Scholar 

  • Debier C, Larondelle Y (2005) Vitamins A and E: metabolism, role and transfer to offspring. Br J Nutr 93:153–174

    Article  CAS  PubMed  Google Scholar 

  • Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91

    Article  Google Scholar 

  • Endler JA (2000) Evolutionary implications of the interaction between animal signals and the environmental. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: signalling and design in animal communication. Tapir Academic Press, Trondheim, Norway, pp 11–46

    Google Scholar 

  • Endler JA, Westcott DA, Madden JR, Robson T (2005) Animal visual systems and the evolution of color patterns; sensory processing illuminates signal evolution. Evolution 50:1795–1818

    Google Scholar 

  • Ewen JG, Thorogood R, Brekke P, Cassey P, Karadas F, Armstrong DP (2009) Maternally invested carotenoids compensate costly ectoparasitism in the hihi. PNAS 106:12798–12802

    Article  CAS  PubMed  Google Scholar 

  • Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a carotenoid-based secondary sexual trait. Science 300:103

    Article  CAS  PubMed  Google Scholar 

  • Friedman A, Sklan D (1997) Effect of dietary fatty acids on humoral immune response of turkeys. Br Poult Sci 38:186–195

    Article  Google Scholar 

  • Gaál A, Csaba G (1998) Testosterone and progesterone level alterations in the adult rat after retinoid (retinol or retinoic acid) treatment (imprinting) in neonatal or adolescent age. Horm Metab Res 30:487–489

    Article  PubMed  Google Scholar 

  • Ganguly J, Mehl JW, Deuel HJ Jr (1953) Studies on carotenoid metabolism. XIII. The carotenoid composition of the blood, liver and ovaries of the rat, ewe, cow, and frog. J Nutr 50:73–83

    CAS  PubMed  Google Scholar 

  • Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  • Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339

    Article  Google Scholar 

  • Hill GE (1999) Is there an immunological cost to carotenoid-based ornamental colouration? Am Nat 154:589–595

    Article  PubMed  Google Scholar 

  • Hill GE (2002) A red bird in a brown bag: the function and evolution of colorful plumage in the house finch. Oxford University Press, Oxford

    Book  Google Scholar 

  • Hill GE (2006) Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, volume 2. Function and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • Hill GE, McGraw KJ (2006) Bird coloration. volume I. Mechanisms and measurements. Harvard University Press, Cambridge

    Google Scholar 

  • Hõrak P, Surai PF, Ots I, Møller AP (2004) Fat soluble antioxidants in brood-rearing great tits: relations to health and appearance. J Avian Biol 35:63–70

    Article  Google Scholar 

  • Karu U, Saks L, Horak P (2008) Carotenoid-based plumage coloration is not affected by vitamin E supplementation in male greenfinches. Ecol Res 23:931–935

    Article  CAS  Google Scholar 

  • Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Am Nat 124:309–323

    Article  Google Scholar 

  • Kuenzel WJ, Rowland AM, Pillai PB, O'Connor-Dennie TI, Emmert JL, Wideman RF (2006) The use of vitamin A-deficient diets and jugular vein ligation to increase intracranial pressure in chickens (Gallus gallus). Poultry Sci 85:537–545

    CAS  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites and sexual selection. Oikos 70:309–311

    Article  Google Scholar 

  • Lucas AM, Stettenheim PR (1972) Avian anatomy. Integument. Agriculture Handbook 362. U.S. Dept. Agric, Washington

    Google Scholar 

  • Martinez A, Rodriguez-Girones MA, BarbosaA CM (2008) Donator acceptor map for carotenoids, melatonin and vitamins. J Physic Chem A 112:9037–9042

    Article  CAS  Google Scholar 

  • Martinez-Padilla J, Mougeot F, Perez-Rodriguez L, Bortolotti GR (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol Letters 3:161–164

    Article  CAS  Google Scholar 

  • Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford

    Google Scholar 

  • McGraw KJ (2004) Colorful songbirds metabolize carotenoid at the integument. J Avian Biol 35:471–476

    Article  Google Scholar 

  • McGraw KJ (2006) Mechanics of carotenoid–based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration. Vol. 1, Function and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • McGraw KJ, Hill GE (2000) Carotenoid based ornamentation and status signalling in house finch. Behav Ecol 11:520–527

    Article  Google Scholar 

  • McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712

    Article  PubMed  Google Scholar 

  • McGraw KJ, Ardia DR (2005) Sex differences in carotenoid status and immune performance in zebra finches. Evol Ecol Res 7:251–262

    Google Scholar 

  • McGraw KJ, Gregory AJ, Parker RS, Adkins-Regan E (2003) Diet, plasma carotenoids and sexual coloration in the zebra finch (Taeniopygia guttata). Auk 120:400–410

    Article  Google Scholar 

  • McGraw KJ, Tourville EA, Butler MW (2008) A quantitative comparison of the commonly used methods for extracting carotenoids from avian plasma. Behav Ecol Sociobiol 62:1991–2002

    Article  Google Scholar 

  • Møller AP (1987) Variation in badge size in male House Sparrows (Passer domesticus): evidence for status signalling. Anim Behav 35:1637–1644

    Article  Google Scholar 

  • Møller AP (1988) Female choice selects for male sexual tail ornaments in the monogamous swallow. Nature 322:996–1005

    Google Scholar 

  • Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence and detoxification ability. Avian Poultry Biol Rev 11:137–159

    Google Scholar 

  • Morales J, Sanz JJ, Moreno J (2006) Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biol Letters 2:334–336

    Article  Google Scholar 

  • Morales J, Velando A, Torres R (2009) Fecundity compromises attractiveness when pigments are scarce. Behav Ecol 20:117–123

    Article  Google Scholar 

  • Negro JJ, Bortolotti 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 12:307–312

    Article  Google Scholar 

  • Ninni P, de Lope F, Saino N, Haussy C, Møller AP (2004) Antioxidants and condition-dependence of arrival date in a migratory passerine. Oikos 105:55–64

    Article  Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  Google Scholar 

  • Pérez MB, Galderón NL, Croci CA (2007) Radiation-induced enhancement of antioxidant activity in extracts of rosemary (Rosmarinus officinalis L.). Food Chem 104:585–592

    Article  CAS  Google Scholar 

  • Perez-Rodriguez L, Viñuela J (2008) Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (Alectoris rufa). Naturwissenschaften 95:821–830

    Article  CAS  PubMed  Google Scholar 

  • Peters A, Denk AG, Dehley K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120

    Article  CAS  PubMed  Google Scholar 

  • Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate traits. Nature 371:598–599

    Article  CAS  Google Scholar 

  • Price DK, Burley NT (1993) Constraints on the evolution of attractive traits: genetic (co)variation of zebra finch bill color. Heredity 71:405–412

    Article  PubMed  Google Scholar 

  • Prota G (1992) Melanins and melanogenesis. Academic Press, San Diego

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol 140A:73–79

    CAS  Google Scholar 

  • Rubenstein DR, Hauber ME (2008) Dynamic feedback between phenotype and physiology in sexually selected traits. Trends Ecol Evol 23:655–658

    Article  PubMed  Google Scholar 

  • Rubenstein DR, Lovette IJ (2009) Reproductive skew selection on female ornamentation in social species. Nature 462:786–789

    Article  CAS  PubMed  Google Scholar 

  • Riley PA (1997) Melanin. Int J Biochem Cell Biol 29:1235–1239

    Article  CAS  PubMed  Google Scholar 

  • Safran RJ, Adelman J, McGraw KJ, Hau M (2008) Sexual signal elaboration affects physiological state in a social vertebrate. Curr Biol 18:461–462

    Article  CAS  Google Scholar 

  • Saks L, McGraw K, Horak P (2003) How feather colour reflect its carotenoid content. Ecology 17:555–561

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. W.H.Freeman, New York

    Google Scholar 

  • Soler JJ, Navarro C, Pérez-Contreras T, Avilés JM, Cuervo JJ (2008) Sexually selected egg coloration in spotless starlings. Am Nat 171:183–194

    Article  PubMed  Google Scholar 

  • Surai PE (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham

    Google Scholar 

  • Surai PE, Kuklenko TV, Ionov IA, Noble RC, Sparks NHC (2000) Effect of Vitamin A on the antioxidant system of the chick during early postnatal development. Brit Poultry Sci 41:454–458

    Article  CAS  Google Scholar 

  • Thurnham DI, Northrop-Clewes CA (1999) Optimal nutrition: vitamin A and the carotenoids. Proc Nutr Soc 58:449–457

    CAS  PubMed  Google Scholar 

  • Veiga JP, Polo V (2008) Fitness consequences of increased testosterone levels in female Spotless Starlings. Am Nat 172:42–53

    Article  PubMed  Google Scholar 

  • Veiga JP, Moreno J, Cordero PJ, Mínguez E (2001) Territory size and polygyny in the spotless starling: resource-holding potential or social inertia? Can J Zool 79:1951–1956

    Article  Google Scholar 

  • Velando A, Beamonte-Barrientos R, Torres R (2006) Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment. Oecologia 149:535–542

    Article  PubMed  Google Scholar 

  • Wallace RS, Teare JA, Diebold E, Michaels M, Willis M (1996) Plasma tocopherol, retinol, and carotenoid concentrations in free-ranging Humboldt penguins in Chile. Zoo Biol 15:127–134

    Article  CAS  Google Scholar 

  • Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice Hall, Englewood Cliffs

    Google Scholar 

Download references

Acknowledgments

We thank A.P. Møller and two anonymous referees for their comments on the manuscript. This research was funded by the Spanish Ministry of Education and Science and European founds (FEDER) (CGL2004-01777/BOS, CGL2007-61251). CN was supported by a predoctoral grant from the Spain's Ministry of Science and Technology (BES-2005-8619). The authorization for carrying out the experimental work on animals in the field was granted by the Dirección General de Gestión del Medio Natural of the Consejería de Medio Ambiente of Junta de Andalucía.

Author information

Authors and Affiliations

  1. Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (CSIC), E-04120, Almería, Spain

    Carlos Navarro, Tomás Pérez-Contreras, Jesús M. Avilés & Juan J. Soler

  2. Departamento de Biología Animal y Ecología, Universidad de Granada, E-18071, Granada, Spain

    Jesús M. Avilés

  3. School of Life Sciences, Arizona State University, Tempe, AZ, 85287-4501, USA

    Kevin J. Mcgraw

Authors
  1. Carlos Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomás Pérez-Contreras
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jesús M. Avilés
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kevin J. Mcgraw
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juan J. Soler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carlos Navarro.

Additional information

Communicated by M. Hauber

An erratum to this article can be found at http://dx.doi.org/10.1007/s00265-010-0978-0

Rights and permissions

Reprints and permissions

About this article

Cite this article

Navarro, C., Pérez-Contreras, T., Avilés, J.M. et al. Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor). Behav Ecol Sociobiol 64, 1057–1067 (2010). https://doi.org/10.1007/s00265-010-0920-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-0920-5

Keywords

Search

Navigation