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Carotenoid-based ornamentation as a dynamic but consistent individual trait

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Abstract

Carotenoid-based ornaments act as signals of quality in many animal species. In contrast to feathers, which are relatively stable structures, carotenoid-pigmented integuments (e.g. bills, lores, tarsi) can change colour rapidly and may better reflect changes in physiological condition. I studied the seasonal variations in plasma carotenoids in red-legged partridges (Alectoris rufa) kept on a constant diet and free of intestinal parasites. Furthermore, I analyzed whether seasonal changes in circulating carotenoids were mirrored by the carotenoid-based coloration of eye rings and bill of this species. Plasma carotenoids showed seasonal variation, with higher levels coinciding with the end of the mating and the start of the laying season. Eye ring pigmentation was related to plasma carotenoid levels, and changes in bill hue (but not changes in UV or red bill chroma) mirrored the variation in plasma carotenoids during the breeding season. Despite the seasonal variation, individual differences in eye ring pigmentation and bill hue, UV and red chroma were consistent throughout the breeding season. Similarly, individual differences in eye ring pigmentation and bill hue and red chroma remained consistent between consecutive years. These results suggest that carotenoid based integumentary colorations act as dynamic traits that accurately reflect the carotenoid-status of individuals, thus reliably indicating consistent differences in individual quality. Furthermore, variability in signal expression appears to have a relevant genetic/phenotypic basis independently of environmental conditions.

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References

  • Allen PC (1992) Effect of coccidiosis on the distribution of dietary lutein in the chick. Poult Sci 71:1457–1463

    PubMed  CAS  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Lond B Biol Sci 274:819–825

    Article  CAS  Google Scholar 

  • Badyaev AV, Duckworth RA (2003) Context-dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird. J Evol Biol 16:1065–1076

    Article  PubMed  CAS  Google Scholar 

  • Blas J, Pérez-Rodríguez L, Bortolotti GR, Viñuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: new 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 Biol Sci 269:29–36

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Bortolotti GR, Negro JJ, Surai PF, Prieto P (2003) Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiol Biochem Zool 76:367–374

    Article  PubMed  CAS  Google Scholar 

  • Bottoni L, Massa R, Lea RW, Sharp PJ (1993) Mate choice and reproductive success in the red-legged partridge (Alectoris rufa). Horm Behav 27:308–317

    Article  PubMed  CAS  Google Scholar 

  • Bright A, Waas JR (2002) Effects of bill pigmentation and UV reflectance during territory establishment in blackbirds. Anim Behav 64:207–213

    Article  Google Scholar 

  • Carter CS (1992) Neuroendocrinology sexual behaviour in the female. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral. A Bradford Book. MIT Press, Cambridge, pp 71–96

    Google Scholar 

  • Cramp S, Simmons KEL (1980) The Birds of the Western Paleartic. Oxford University Press, Oxford

    Google Scholar 

  • Dawson RD, Bortolotti GR (2006) Carotenoid-dependent coloration of male American kestrels predicts ability to reduce parasitic infections. Naturwissenschaften 93:597–602

    Article  PubMed  CAS  Google Scholar 

  • Dresp B, Jouventin P, Langley K (2005) Ultraviolet reflecting photonic microstructures in the King Penguin beak. Biol Lett 1:310–313

    Article  PubMed  Google Scholar 

  • Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Geenfield MD, Rodríguez RL (2004) Genotype-environmnet interaction and the reliability of mating signal. Anim Behav 68:1461–1468

    Article  Google Scholar 

  • Grill CP, Moore AJ (1998) Effects of larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia 114:274–282

    Article  Google Scholar 

  • Hadfield JD, Owens IPF (2006) Strong environmental determination of a carotenoid-based plumage trait is not mediated by carotenoid availability. J Evol Biol 19:1104–1114

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Hill GE (2002) A red bird in a brown bag. Oxford University Press, Oxford

    Google Scholar 

  • Hill GE, McGraw KJ (eds) (2006) In: Bird coloration, vol. 2, Function. and evolution. Harvard University Press, Cambridge

  • Hõrak P, Ots I, Vellau H, Spottiswoode C, Møller AP (2001) Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126:166–176

    Article  Google Scholar 

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

    Google Scholar 

  • Littell RC, Henry PR, Ammerman CB (1998) Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76:1216–1231

    PubMed  CAS  Google Scholar 

  • Martínez-Padilla J, Mougeot F, Pérez-Rodríguez L, Bortolotti GR (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol Lett 3:161–164

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • McGraw KJ (2006) Sex steroid dependence of carotenoid-based coloration in female zebra finches. Physiol Behav 88:347–352

    Article  PubMed  CAS  Google Scholar 

  • McGraw KJ, Hill GE (2001) Carotenoid acces and intraspecific variation in plumage pigmentation in American goldfinches (Carduelis tristis) and Northern cardinals (Cardinalis cardinalis). Funct Ecol 15(15):732–739

    Article  Google Scholar 

  • McGraw KJ, Gergory AJ (2004) Carotenoid pigments in American goldfinches: what is the optimal biochemical strategy for becoming colourful? Biol J Linn Soc 83:273–280

    Article  Google Scholar 

  • McGraw KJ, Hill GE, Navara KJ, Parker RS (2004) Differential accumulation and pigmenting ability of dietary carotenoids in colourful finches. Physiol Biochem Zool 77:484–491

    Article  PubMed  CAS  Google Scholar 

  • McGraw KJ, Hudon J, Hill GE, Parker RS (2005) A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments on animal tissues. Behav Ecol Sociobiol 57:391–397

    Article  Google Scholar 

  • McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colourful songbird. Behav Ecol Sociobiol 60:117–122

    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 Poultry Sci Rev 11:137–159

    Google Scholar 

  • Mougeot F, Martínez-Padilla J, Pérez-Rodríguez L, Bortolotti GR (2007a) Carotenoid-based coloration and ultraviolet reflectance of the sexual ornaments of grouse. Behav Ecol Sociobiol 61:741–751

    Article  Google Scholar 

  • Mougeot F, Pérez-Rodríguez L, Martínez-Padilla J, Leckie F, Redpath SM (2007b) Parasites, testosterone and honest carotenoid-based signaling of health. Funct Ecol. 21:886–898

    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 

  • Negro JJ, Tella JL, Hiraldo F, Bortolotti GR, Prieto P (2001) Sex- and age-related variation in plasma carotenoids despite a constant diet in the red-legged partridge Alectoris rufa. Ardea 89:275–280

    Google Scholar 

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

    Article  Google Scholar 

  • Omland KE (1996) Female mallard male preferences for multiple male preferences. II Experimental variation. Behav Ecol Sociobiol 39:361–366

    Article  Google Scholar 

  • Pärt T, Qvanström A (1997) Badge size in collared flycatchers predict the outcome of male competition over territories. Anim Behav 54:893–899

    Article  Google Scholar 

  • Pérez-Rodríguez L, Blas J, Viñuela J, Marchant TA, Bortolotti GR (2006) Condition and androgen levels: are condition-dependent and androgen-mediated traits two sides of the same coin? Anim Behav 72:97–103

    Article  Google Scholar 

  • Pérez-Rodríguez L, Alonso-Álvarez C, Viñuela J (2007) Repeated sampling but not sampling hour affects plasma carotenoid levels. Physiol Biochem Zool 80:250–254

    Article  PubMed  Google Scholar 

  • Rintamaki PT, Hoglund J, Karvonen E, Alatalo RV, Bjorklund N, Lundberg A, Ratti O, Vouti J (2000) Combs and sexual selection in black grouse (Tetrao tetrix). Behav Ecol 11:465–471

    Article  Google Scholar 

  • Rosen RF, Tarvin KA (2006) Sexual signals of the male American goldfinch. Ethology 108:1008–1019

    Article  Google Scholar 

  • Saks L, McGraw KJ, Hõrak P (2003) How feather color reflects its carotenoid content. Funct Ecol 17:555–561

    Article  Google Scholar 

  • Senar JC, Quesada J (2006) Absolute and relative signal: a comparison between melanin- and carotenoid-based patches. Behaviour 143:589–595

    Article  Google Scholar 

  • Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Florida

    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 149:135–142

    Article  Google Scholar 

  • Villafuerte R, Negro JJ (1998) Digital imaging for colour measurement in ecological research. Ecol Lett 1:151–154

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

I am grateful to Gary R. Bortolotti, François Mougeot, Javier Viñuela and two anonymous referees for their valuable comments on a first version of the manuscript, and Beatriz Arroyo for reviewing the English. I also thank Fernando, Emiliano and Salvador J. Luna for their help in maintenance of birds and data collection. Financial support was provided by the Research Project PAI-02–006 of the Junta de Comunidades de Castilla-La Mancha. I was supported by a FPU grant from the Spanish Ministerio de Educación y Ciencia. This study was performed according to Spanish laws.

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  1. Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC, UCLM, JCCM), Ronda de Toledo, s/n, E-13071, Ciudad Real, Spain

    Lorenzo Pérez-Rodríguez

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Correspondence to Lorenzo Pérez-Rodríguez.

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Communicated by: K. McGraw

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Figure S1

The following pictures illustrate the five-level scale employed to assess aye-ring pigmentation in red-legged partridges. This scale represents differences in colour that were large enough to be easily detected in the entire picture set. This colour scoring method allowed me to detect only large differences in coloration, so the results reported here are conservative. A similar scoring method has been successfully employed in this species to evaluate the relationship between eye ring pigmentation and body condition (Pérez Rodríguez and Viñuela, submitted). To evaluate scoring repeatability, 30 pictures were collected in duplicate and scored twice by me, finding a 96.6% of coincidence in scoring. Furthermore, a subsample of 75 pictures were independently scored by me and another person unaware of the experimental design, finding that 78 % of the scores given to the pictures were coincident, 19% of them differed in one point of the scale between scorers and only 3% differed in two points. Thus, colour scores were reliable and repeatable. (DOC 106 KB)

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Pérez-Rodríguez, L. Carotenoid-based ornamentation as a dynamic but consistent individual trait. Behav Ecol Sociobiol 62, 995–1005 (2008). https://doi.org/10.1007/s00265-007-0527-7

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