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.
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
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
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
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
Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339
Hill GE, Farmer KL (2005) Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92:30–34
Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634
Hill GE (2014) Cellular respiration: the nexus of stress, condition, and ornamentation. Integr Comp Biol 54:645–657
Kohl KD (2012) Diversity and function of the avian gut microbiota. J Comp Physiol B 182:591–560
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
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
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
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
McGraw KJ, Hill GE (2000) Carotenoid-based ornamentation and status signaling in the house finch. Behav Ecol 11:520–527
McGraw KJ, Parker RS (2005) A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird. Physiol Behav 87:103–108
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
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
Nespolo RF, Franco M (2007) Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J Exp Biol 210:3877–3878
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
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
Svensson P, Wong B (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189
Toews DPL, Hofmeister NR, Taylor SA (2017) The evolution and genetics of carotenoid processing in animals. Trends Genet 33:171–182
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
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
Corresponding author
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
About this article
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
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-017-1516-y