Skip to main content
SpringerLink
Log in

Carotenoid supplementation and sex-specific trade-offs between colouration and condition in common tern chicks

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Carotenoids, as pigments with antioxidant and immunoregulatory properties, play a crucial role in developing chicks. Carotenoids must be acquired through diet and are relatively scarce, suggesting that their availability is a limiting factor leading to a trade-off between colour displays and physiological functions. However, potential differences in this trade-off between male and female chicks have been little studied. We manipulated carotenoid availability in 9 days old common tern Sterna hirundo chicks by supplementing their fish diet with four carotenoids during 9 days. Our aim was to examine sex-specific responses to the experimental increase of dietary carotenoids on plasma circulation, physiological and condition variables and successful fledging. Furthermore, to explore the functional and evolutionary basis of the trade-off, we studied the relationships among carotenoid concentration, mediated immune response and foot colouration. After treatment, control chicks showed decreasing plasma levels for most carotenoid types, whereas supplemented chicks had strong increases. Colour luminosity and saturation increased in both treatment groups, while hue only changed significantly towards redder feet in supplemented females. Supplemented chicks presented neither different T-cell-mediated immunity nor other differences compared to control chicks. Nevertheless, supplemented females showed tendencies towards decreased immune responses and increased δ15N signatures, and supplemented males towards greater body mass. Our results indicate colouration may have, in females, a signalling function as to compensate for immunological costs. In males, additional availability of carotenoids may contribute to improve the body condition. This study suggests that trade-off responses to carotenoid availability are sex-specific in tern chicks. Thus, parental carotenoid supply to chicks may be an unrecognised component in sex allocation.

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

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

    Article  PubMed  Google Scholar 

  • Badyaev AV, Seaman DA, Navara KJ, Hill GE, Mendonça MT (2006) Evolution of sex-biased maternal effects in birds. III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. J Evol Biol 19:1044–1057

    Article  PubMed  CAS  Google Scholar 

  • Becker PH (1998) Langzeittrends des Bruterfolgs der Flußseeschwalbe Sterna hirundo und seiner Einflußgrößen im Wattenmeer. Vogelwelt 119:223–234

    Google Scholar 

  • Becker PH, Ludwigs JD (2004) Sterna hirundo Common Tern. In: Parkin D (ed) BWP update vol 6 nos 1/2. Oxford University Press, London, pp 93–139

    Google Scholar 

  • Becker PH, Wendeln H (1997) A new application for transponders in population ecology of the Common Tern. Condor 99:534–538

    Article  Google Scholar 

  • Becker PH, Wink M (2003) Influences of sex, sex composition of brood and hatching order on mass growth in Common Terns Sterna hirundo. Behav Ecol Sociobiol 54:136–146

    Google Scholar 

  • Becker PH, Wendeln H, González-Solís J (2001) Population dynamics, recruitment, individual quality and reproductive strategies in common terns Sterna hirundo marked with transponders. Ardea 89(Special issue):241–252

    Google Scholar 

  • Berthouly A, Helfenstein F, Tanner M, Richner H (2008) Sex-related effects of maternal egg investment on offspring in relation to carotenoid availability in the great tit. J Anim Ecol 77:74–82

    Article  PubMed  Google Scholar 

  • Blas J, Pérez-Rodriguez L, Bortolotti GR, Vinuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc Natl Acad Sci USA 103:18633–18637

    Article  PubMed  CAS  Google Scholar 

  • Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002) Carotenoids and egg quality in the lesser black-backed gull (Larus fuscus): a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36

    Article  CAS  Google Scholar 

  • Cabana G, Rasmussen JB (1994) Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372:255–257

    Article  CAS  Google Scholar 

  • Casagrande S, Costantini D, Fanfani A, Tagliavini J, Dell’Omo G (2007) Patterns of serum carotenoid accumulation and skin color variation in kestrel nestlings in relation to breeding conditions and different terms of carotenoid supplementation. J Comp Physiol B 177:237–245

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Costantini D, Fanfani A, Dell’Omo G (2007) Carotenoid availability does not limit the capability of nestling kestrels (Falco tinnunculus) to cope with oxidative stress. J Exp Biol 210:1238–1244

    Article  PubMed  CAS  Google Scholar 

  • Cucco M, Guasco B, Malacarne G, Ottonelli R (2006) Effects of β-carotene supplementation on chick growth, immune status and behaviour in the grey partridge, Perdix perdix. Behav Process 73:325–332

    Article  CAS  Google Scholar 

  • de Ayala RM, Martinelli R, Saino N (2006) Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica). Behav Ecol Sociobiol 60:619–630

    Article  Google Scholar 

  • de Ayala RM, Saino N, Møller AP, Anselmi C (2007) Mouth coloration of nestlings covaries with offspring quality and influences parental feeding behavior. Behav Ecol 18:526–534

    Article  Google Scholar 

  • Forero MG, Tella JL, Hobson KA, Bertellotti M, Blanco G (2002) Conspecific food competition explains variability in colony size: a test in Magellanic Penguins. Ecology 83:3466–3475

    Article  Google Scholar 

  • Frank D (1992) The influence of feeding conditions on food provisioning of chicks in Common Terns Sterna hirundo nesting in the German Wadden Sea. Ardea 80:45–55

    Google Scholar 

  • Goodwin TW (1984) The biochemistry of the carotenoids. Volume II. Animals. Chapman & Hall, London

    Google Scholar 

  • Goodwin TW (1986) Metabolism, nutrition, and function of carotenoids. Annu Rev Nutr 6:273–297

    Article  PubMed  CAS  Google Scholar 

  • Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322

    Article  CAS  Google Scholar 

  • Griggio M, Morosinotto C, Pilastro A (2009) Nestlings’ carotenoid feather ornament affects parental allocation strategy and reduces maternal survival. J Evol Biol 22:2077–2085

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hill GE (1992) Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109:1–12

    Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes. II. Factors influencing diet-tissue fractionation. Condor 94:187–195

    Google Scholar 

  • Hobson KA, Clark RG (1993) Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641

    Google Scholar 

  • Hudon J, Brush AH (1990) Identification of carotenoid pigments in birds. Methods Enzymol 213:312–321

    Article  Google Scholar 

  • Kilner RM (2006) Function and evolution of color in young birds. In: Hill GE, McGraw KJ (eds) Bird coloration. Volume II. Function and evolution. Harvard University Press, London, pp 201–232

    Google Scholar 

  • Kristiansen KO, Bustnes JO, Folstad I, Helberg M (2006) Carotenoid coloration in great black-backed gull Larus marinus reflects individual quality. J Avian Biol 37:6–12

    Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    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, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92:375–380

    Article  PubMed  CAS  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, 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 Poult Biol Rev 11:137–159

    Google Scholar 

  • Møller AP, Flensted-Jensen E, Mardal W (2007) Black beak tip coloration as a signal of phenotypic quality in a migratory seabird. Behav Ecol Sociobiol 61:1561–1571

    Article  Google Scholar 

  • Neubauer W (1978) Experimentelle Untersuchungen zur akustischen und visuellen Kommunikation an der Flußseeschwalbe (Sterna hirundo L.) unter besonderer Berücksichtigung der Jungenaufzucht. Dissertation, Humboldt-Universität, Berlin

  • Olson VA, Owens IPF (2005) Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny. J Evol Biol 18:1534–1546

    Article  PubMed  CAS  Google Scholar 

  • Romano M, Caprioli M, Ambrosini R, Rubolini D, Fasola M, Saino N (2008) Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order. J Evol Biol 21:1626–1640

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Ninni P, Calza S, Martinelli R, de Bernardi F, Møller AP (2000) Better red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings. Proc R Soc Lond B Biol Sci 267:57–61

    Article  CAS  Google Scholar 

  • Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2003) Maternal antibodies but not carotenoids in barn swallow eggs covary with embryo sex. J Evol Biol 16:516–522

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Bertacche V, Bonisoli Alquati A, Romano M, Rubolini D (2008) Phenotypic correlates of yolk and plasma carotenoid concentration in yellow-legged gull chicks. Physiol Biochem Zool 81:211–225

    Article  PubMed  Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Article  Google Scholar 

  • Stradi R (1998) The colour of flight: carotenoids in bird plumage. Solei Gruppo Editoriale Informatico, Milan

    Google Scholar 

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

    Google Scholar 

  • Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651

    Article  CAS  Google Scholar 

  • Surai PF, Speake BK, Wood NAR, Blount JD, Bortolotti GR, Sparks NHC (2001) Carotenoid discrimination by the avian embryo: a lesson from wild birds. Comp Biochem Physiol B 128:743–750

    Article  PubMed  CAS  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2005) Carotenoid-based nestling colouration and parental favouritism in the great tit. Oecologia 143:477–482

    Article  PubMed  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 

  • Verboven N, Evans NP, D’Alba L, Nager RG, Blount JD, Surai PF, Monaghan P (2005) Intra-specific interactions influence egg composition in the lesser-black gull (Larus fuscus). Behav Ecol Sociobiol 57:357–365

    Article  Google Scholar 

  • Wagener M (1998) Praktische Hinweise für brutbiologische Untersuchungen an der Flußseeschwalbe Sterna hirundo. Vogelwelt 119:279–286

    Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the “Banter See team” in 2006, especially J. Sprenger. We are also grateful to J.M. Vilanova (Kemin Iberica) and R. Tena (DSM Nutritional Products) for kindly supplying dietary carotenoid supplements free of charges; to the Research Centre TERRAMARE, U. Pijanowska, and F. Bairlein for providing logistical and technical support, and to B. Metzger for invaluable help during the whole process. M.M.B. was supported by a postgraduate grant of the Generalitat de Catalunya (Spain) and J.G-S. was supported by a contract of the Program Ramon y Cajal funded by the Ministerio de Educación y Ciencia and Fondos FEDER. This project was done under licence of LAVES, Oldenburg, of the Stadt Wilhelmshaven and financially supported by the Deutsche Forschungsgemeinschaft (BE 916/8-2).

Author information

Authors and Affiliations

  1. Institut de Recerca de la Biodiversitat (IRBio), Department Biologia Animal (Vertebrats), Universitat de Barcelona, Av. Diagonal 645, Barcelona, 08028, Spain

    María M. Benito & Jacob González-Solís

  2. Institut für Vogelforschung “Vogelwarte Helgoland”, An der Vogelwarte 21, Wilhelmshaven, 26386, Germany

    Peter H. Becker

Authors
  1. María M. Benito
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacob González-Solís
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter H. Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María M. Benito.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benito, M.M., González-Solís, J. & Becker, P.H. Carotenoid supplementation and sex-specific trade-offs between colouration and condition in common tern chicks. J Comp Physiol B 181, 539–549 (2011). https://doi.org/10.1007/s00360-010-0537-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0537-z

Keywords

Search

Navigation