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Carotenoids increase immunity and sex specifically affect color and redox homeostasis in a monochromatic seabird

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Abstract

Carotenoid-based integument coloration is extremely widespread in animals and commonly used as an honest signal of condition in sexual selection. Besides being used for color expression, carotenoids have antioxidant and immunomodulatory activity. Being a limited resource, carotenoid allocation to competing demands generates a trade-off. Recent studies, however, suggest that the antioxidant role of carotenoids might not be as important as previously thought. To shed light on the mechanism maintaining carotenoid-based signal honesty in the black-legged kittiwake (Rissa tridactyla), we supplemented males and females with dietary yellow xanthophylls (lutein and zeaxanthin) during the chick-rearing period, when male coloration may be a good indicator of future reproductive success. The supplementation affected plasma carotenoid levels similarly in males and females, i.e., it increased the levels of lutein but decreased the levels of total astaxanthin, one of the main pigments coloring integuments in this species. Supplemented adults and their chicks had stronger immune response than controls, suggesting that yellow xanthophylls enhance the innate immune system in kittiwakes. However, supplementation caused sex-specific effects on integument coloration and oxidative stress. Supplemented males had duller integuments, but similar oxidative damages compared to control males, while supplemented females had more colorful integuments, but higher oxidative damages than control females. Because the increase in lutein was associated with a decrease in other potential antioxidants (i.e., astaxanthin and vitamin A), the role of carotenoids as antioxidants in kittiwakes remains undetermined. Our results, however, indicate that the trade-off responses to carotenoid availability are sex-specific in kittiwakes.

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Acknowledgments

We thank Kemin Food for kindly providing carotenoids. We are very grateful to N. Vetter, and V. Frochot for their help in the field, and F. Helfenstein for helpful discussion. We thank C. Alonso-Alvarez and two anonymous referees for their valuable comments on the manuscript. This study was financed, in part, by the French Polar Institute Paul-Emile Victor (IPEV, program 1162) and the Cambridge Infectious Diseases Consortium (CIDC). This work originated in the lab EDB as part of the ‘Laboratoire d’Excellence’ (LABEX) entitled TULIP (ANR-10-LABX-41). Any use of trade names is for descriptive purposes only and does not imply endorsement by the US government.

Ethical standards

Experiments were approved by the US Fish and Wildlife Service and State of Alaska.

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Author notes

  1. Scott A. Hatch

    Present address: Institute for Seabird Research and Conservation, 12850 Mountain Place, Anchorage, AK, 99516, USA

Authors and Affiliations

  1. UPS, EDB (Laboratoire Evolution et Diversité Biologique), UMR5174, CNRS, 118 route de Narbonne, 31062, Toulouse, France

    Sarah Leclaire, Pierrick Blanchard, Christophe de Franceschi, Thomas Merkling & Étienne Danchin

  2. EDB, UMR5174, Université de Toulouse, 31062, Toulouse, France

    Sarah Leclaire, Pierrick Blanchard, Christophe de Franceschi, Thomas Merkling & Étienne Danchin

  3. Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS, 1919 route de Mende, 34293, Montpellier, France

    Sarah Leclaire

  4. Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge, CB3 0ES, UK

    Vincent Bourret

  5. U.S. Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, AK, 99508, USA

    Scott A. Hatch

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Leclaire, S., Bourret, V., Blanchard, P. et al. Carotenoids increase immunity and sex specifically affect color and redox homeostasis in a monochromatic seabird. Behav Ecol Sociobiol 69, 1097–1111 (2015). https://doi.org/10.1007/s00265-015-1922-0

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