Skip to main content
Log in

Carotenoid coloration is related to fat digestion efficiency in a wild bird

  • Short Communication
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

Some of the most spectacular visual signals found in the animal kingdom are based on dietarily derived carotenoid pigments (which cannot be produced de novo), with a general assumption that carotenoids are limited resources for wild organisms, causing trade-offs in allocation of carotenoids to different physiological functions and ornamentation. This resource trade-off view has been recently questioned, since the efficiency of carotenoid processing may relax the trade-off between allocation toward condition or ornamentation. This hypothesis has so far received little exploratory support, since studies of digestive efficiency of wild animals are limited due to methodological difficulties. Recently, a method for quantifying the percentage of fat in fecal samples to measure digestive efficiency has been developed in birds. Here, we use this method to test if the intensity of the carotenoid-based coloration predicts digestive efficiency in a wild bird, the house finch (Haemorhous mexicanus). The redness of carotenoid feather coloration (hue) positively predicted digestion efficiency, with redder birds being more efficient at absorbing fats from seeds. We show for the first time in a wild species that digestive efficiency predicts ornamental coloration. Though not conclusive due to the correlative nature of our study, these results strongly suggest that fat extraction might be a crucial but overlooked process behind many ornamental traits.

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.

Institutional subscriptions

Fig. 1

References

  • Brawner WR, Hill GE, Sundermann CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male house finches. Auk 117:952–963

    Article  Google Scholar 

  • Caviedes-Vidal E, McWhorter TJ, Lavin SR, Chediack JG, Tracy CR, Karasov WH (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. P Natl Acad Sci USA 104:19132–19137

    Article  CAS  Google Scholar 

  • Galvan I, Garrido-Fernandez J, Rios J, Perez-Galvez A, Rodriguez-Herrera B, Negro JJ (2016) Tropical bat as mammalian model for skin carotenoid metabolism. P Natl Acad Sci USA 113:10932–10937

    Article  CAS  Google Scholar 

  • Giraudeau M, Mousel M, Earl S, McGraw K (2014) Parasites in the City: degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus). PLoS ONE 9:e86747

  • Di Mascio P, Murphy ME, Sies H (1991) Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols. Am J Clin Nutr 53:194–200

    Google Scholar 

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

    Article  Google Scholar 

  • Hill GE, Farmer KL (2005) Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92:30–34

    Article  CAS  PubMed  Google Scholar 

  • Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634

    Article  PubMed  Google Scholar 

  • Hill GE (2014) Cellular respiration: the nexus of stress, condition, and ornamentation. Integr Comp Biol 54:645–657

    Article  PubMed  Google Scholar 

  • Kohl KD (2012) Diversity and function of the avian gut microbiota. J Comp Physiol B 182:591–560

    Article  PubMed  Google Scholar 

  • Krajmalnik-Brown R, Ilhan Z-E, Kang D-W, DiBaise JK (2012) Effects of gut microbes on nutrient absorption and energy regulation. Nutr Clin Pract 27:201–214

    Article  PubMed  PubMed Central  Google Scholar 

  • Lendvai ÁZ, Giraudeau M, Németh J, Bakó V, McGraw KJ (2013) Carotenoid-based plumage coloration reflects feather corticosterone levels in male house finches (Haemorhous mexicanus). Behav Ecol Sociobiol 67:1817–1824

    Article  Google Scholar 

  • Madonia C, Hutton P, Giraudeau M, Sepp T (2017) Data from: carotenoid coloration is related to fat digestion efficiency in a wild bird. Dryad Digital Repository. https://doi.org/10.5061/dryad.s7q28

  • Major RJJ, Ruff MD (1978) Eimeria spp.: influence of coccidia on digestion (amylolytic activity) in broiler chickens. Exp Parasitol 45:234–240

    Article  CAS  PubMed  Google Scholar 

  • McGraw KJ, Adkins-Regan E, Parker RS (2002) Anhydrolutein in the zebra finch: a new, metabolically derived carotenoid in birds. Comp Biochem Phys 132:811–818

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • McGraw KJ, Parker RS (2005) A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird. Physiol Behav 87:103–108

    Article  PubMed  Google Scholar 

  • McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration. Mechanisms and measurements, vol. 1. Harvard University Press, Cambridge, MA, pp 177–242

    Google Scholar 

  • Meitern R, Lind MA, Karu U, Hõrak P (2016) Simple and noninvasive method for assessment of digestive efficiency: validation of fecal steatocrit in greenfinch coccidiosis model. Ecol Evol 6:8756–8763

    Article  PubMed  PubMed Central  Google Scholar 

  • Nespolo RF, Franco M (2007) Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J Exp Biol 210:3877–3878

    Article  Google Scholar 

  • Perez-Rodriguez L, Mougeot F, Alonso-Alvarez C (2010) Carotenoid-based coloration predicts resistance to oxidative damage during immune challenge. J Exp Biol 213:1685–1690

    Article  CAS  PubMed  Google Scholar 

  • Simons MJP, Cohen AA, Verhulst S (2012) What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds? A meta-analysis. PLoS One 7:e43088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svensson P, Wong B (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189

    Article  Google Scholar 

  • Toews DPL, Hofmeister NR, Taylor SA (2017) The evolution and genetics of carotenoid processing in animals. Trends Genet 33:171–182

    Article  CAS  PubMed  Google Scholar 

  • Tran M, Forget P, Vandenneucker A, Strik J, Vankreel B, Kuijten R (1994) The acid steatocrit—a much improved method. J Pediatr Gastr Nutr 19:299–303

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Devon Allred, Aaron Craig, Brittany Switzer, Randi Bromm, Kevin McGraw, Peeter Hõrak, and Richard Meitern for help and advice. The publication reflects only the authors’ views; the Research Executive Agency is not responsible for any use that may be made of the information it contains.

Funding

This study was supported by the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No 701747 to T.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christina Madonia.

Ethics declarations

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This research was approved by ASU Institutional Animal Care and Use Committee by animal protocol number 15-1401RRFC43.

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Communicated by: Alexandre Roulin

Electronic supplementary material

ESM 1

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Madonia, C., Hutton, P., Giraudeau, M. et al. Carotenoid coloration is related to fat digestion efficiency in a wild bird. Sci Nat 104, 96 (2017). https://doi.org/10.1007/s00114-017-1516-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-017-1516-y

Keywords

Navigation