Abstract
Carotenoid-based signals may function as indicators of individual quality because, being exclusively obtained from the diet, they indicate the ability of individuals to intake high-quality food. Moreover, carotenoids are involved in several important physiological functions, including antioxidant defense, so that carotenoid-based colorations have been suggested to reflect the antioxidant status of their bearers. The present correlative, cross-sectional study aimed at investigating if the skin carotenoid-based coloration is a signal of antioxidant defenses in the brown trout (Salmo trutta Linnaeus, 1758). We investigated the relationships between carotenoid-based coloration traits (including the number, density and redness of red spots, as well as the ventral yellowness), and both non-enzymatic (plasma and liver total antioxidant capacity) and enzymatic antioxidant defenses (activity of hepatic superoxide dismutase —SOD, catalase —CAT and glutathione peroxidase —GPx). We found significant positive covariations between antioxidant defenses and carotenoid-based skin coloration, in terms of ventral yellowness. Brown trout individuals displaying intense carotenoid-based coloration (i.e., ventral yellowness) had a high non-enzymatic antioxidant capacity both in plasma and in liver and, interestingly, an elevated activity of hepatic SOD and CAT. Our data suggest that carotenoid-based skin colorations may be considered a signal of individual quality in terms of antioxidant defenses in the brown trout.
Similar content being viewed by others
References
Alonso-Alvarez, C., S. Bertrand, G. Devevey, J. Prost, B. Faivre & G. Sorci, 2004. Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecology Letters 7: 363–368.
Aparicio, E., E. Garcia-Berthou, R. M. Araguas, P. Martinez & J. L. Garcia-Marin, 2005. Body pigmentation pattern to assess introgression by hatchery stocks in native Salmo trutta from Mediterranean streams. Journal of Fish Biology 67: 931–949.
Backström, T., E. Brännäs, J. Nilsson & C. Magnhagen, 2014. Behaviour, physiology and carotenoid pigmentation in Arctic charr Salvelinus alpinus. Journal of Fish Biology 84: 1–9.
Bagnara, J. T., 1998. Comparative anatomy and physiology of pigment cells in nonmammalian tissues. In Nordland, J., R. Boissy, V. Hearing, R. King & J. Ortonne (eds), The Pigmentary System. Physiology and Pathophysiology. Oxford University Press, New York: 9–40.
Balshine, S., 2012. Patterns of parental care in vertebrates. In Royle, N., P. Smiseth & M. Kölliker (eds), The Evolution of Parental Care. Oxford University Press, Oxford: 62–80.
Bertrand, S., B. Faivre & G. Sorci, 2006. Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants? Journal of Experimental Biology 209: 4414–4419.
Birnie-Gauvin, K., D. Costantini, S. J. Cooke & W. G. Willmore, 2017. A comparative and evolutionary approach to oxidative stress in fish: a review. Fish and Fisheries 18: 928–942.
Bjerkeng, B., T. Storebakken & S. Liaaen-Jensen, 1992. Pigmentation of rainbow-trout from start feeding to sexual-maturation. Aquaculture 108: 333–346.
Blanc, J. M., H. Poisson & R. Vibert, 1982. Variabilite genetique de la ponctuation noire sur la truitelle Fario (Salmo trutta L.). Annales De Genetique Et De Selection Animale 14: 225–236.
Blanc, J. M., B. Chevassus & F. Krieg, 1994. Inheritance of the number of red spots on the skin of the brown trout. Aquatic Living Resources 7: 133–136.
Blomhoff, R., & H. K. Blomhoff, 2006. Overview of retinoid metabolism and function. Developmental Neurobiology 66(7): 606–630.
Blount, J. D., D. C. Houston & A. P. Møller, 2000. Why egg yolk is yellow. Trends in Ecology & Evolution 15: 47–49.
Boonstra, R., 2013. Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Functional Ecology 27(1): 11–23.
Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry 72(1–2): 248–254.
Brown, A. C., H. M. Leonard, K. J. McGraw & E. D. Clotfelter, 2014. Maternal effects of carotenoid supplementation in an ornamented cichlid fish (Amantitlania siquia). Functional Ecology 28: 612–620.
Bud, I., I. L. Dombi, & V. V. Vlădău, 2009. The geographic isolation impact on evolution of some morpho-physiological features in the Brown trout (Salmo trutta fario Linnaeus). AACL Bioflux 2: 31–50.
Burton, G. W. & K. U. Ingold, 1984. β-carotene: an unusual type of lipid antioxidant. Science 224: 569–573.
Candolin, U. & L. Tukiainen, 2015. The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments? Proceedings of the Royal Society of London. Series B, Biological Sciences 282: 1–9.
Catoni, C., A. Peters & H. M. Schaefer, 2008. Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Animal Behaviour 76: 1107–1119.
Costantini, D. & A. P. Møller, 2008. Carotenoids are minor antioxidants for birds. Functional Ecology 22: 367–370.
Craig, J. K., C. J. Foote & C. C. Wood, 2005. Countergradient variation in carotenoid use between sympatric morphs of sockeye salmon (Oncorhynchus nerka) exposes nonanadromous hybrids in the wild by their mismatched spawning colour. Biological Journal of the Linnean Society 84: 287–305.
Dale, J., C. J. Dey, K. Delhey, B. Kempenaers & M. Valcu, 2015. The effects of life history and sexual selection on male and female plumage colouration. Nature 527: 367–370.
Djurdjevič, I., M. E. Kreft & S. Sušnik Bajec, 2015. Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids. Journal of Anatomy 227: 583–595.
Endler, J. A., 1980. Natural-selection on color patterns in Poecilia reticulata. Evolution 34: 76–91.
Erel, O., 2004. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clinical Biochemistry 37: 277–285.
Fujii, R., 2000. The regulation of motile activity in fish chromatophores. Pigment Cell Research 13: 300–319.
Garner, S. R., B. D. Neff & M. A. Bernards, 2010. Dietary carotenoid levels affect carotenoid and retinoid allocation in female Chinook salmon Oncorhynchus tshawytscha. Journal of Fish Biology 76: 1474–1490.
Halliwell, B., 1996. Vitamin C: antioxidant or pro-oxidant in vivo? Free Radical Research 25: 439–454.
Hartley, R. C. & M. W. Kennedy, 2004. Are carotenoids a red herring in sexual display? Trends in Ecology & Evolution 19: 353–354.
Hubbard, J. K., J. A. C. Uy, M. E. Hauber, H. E. Hoekstra & R. J. Safran, 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends in Genetics 26: 231–239.
Ibrahim, A., C. Shimizu & M. Kono, 1984. Pigmentation of cultured red sea bream, Chrysophrys major, using astaxanthin from Antarctic krill, Euphausia superba, and a mysid, Neomysis sp. Aquaculture 38: 45–57.
Johnstone, R. A., 1997. The evolution of animal signals. In Krebs, J. R. & N. B. Davies (eds), Behavioural ecology: an evolutionary approach. Blackwell Scientific Publications, Oxford: 155–178.
Kelsh, R. N., 2004. Genetics and evolution of pigment patterns in fish. Pigment Cell Research 17: 326–336.
Kim, S.-Y. & A. Velando, 2016. Genetic conflict between sexual signaling and juvenile survival in the three-spined stickleback. BMC Evolutionary Biology 16: 1–7.
Kocabaş, M., M. Kayim, E. Can, M. Ateş & F. Kutluyer, 2011. Spotting pattern features in the brown trout (Salmo trutta macrostigma, T., 1954) population. Scientific Research and Essays 6: 5021–5024.
Kolluru, G. R., G. F. Grether, S. H. South, E. Dunlop, A. Cardinali, L. Liu & A. Carapiet, 2006. The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biological Journal of the Linnean Society 89(2): 301–309.
Kop, A. & Y. Durmaz, 2008. The effect of synthetic and natural pigments on the colour of the cichlids (Cichlasoma severum sp., Heckel 1840). Aquaculture International 16: 117–122.
Krinsky, N. I., 1989. Antioxidant functions of carotenoids. Free Radical Biology Medicine 7: 617–635.
Krinsky, N. I., 1993. Actions of carotenoids in biological systems. Annual Review of Nutrition 13(1): 561–587.
Krinsky, N. I., & K. J. Yeum, 2003. Carotenoid–radical interactions. Biochemical and Biophysical Research Communications 305(3): 754–760.
Leclercq, E., J. F. Taylor & H. Migaud, 2010. Morphological skin colour changes in teleosts. Fish and Fisheries 11: 159–193.
León, K., D. Mery, F. Pedreschi & J. León, 2006. Color measurement in L∗a∗b∗ units from RGB digital images. Food Research International 39: 1084–1091.
Li, M. H., E. H. Robinson, D. F. Oberle & P. V. Zimba, 2007. Effects of various dietary carotenoid pigments on fillet appearance and pigment absorption in channel catfish Ictalarus punctatus. Journal of the World Aquaculture Society 38: 557–563.
Lozano, G. A., 1994. Carotenoids, parasites, and sexual selection. Oikos 70: 309–311.
Lozano, G. A., 2001. Carotenoids, immunity, and sexual selection: comparing apples and oranges?. The American Naturalist 158(2): 200–203.
Lushchak, V. I., 2011. Environmentally induced oxidative stress in aquatic animals. Aquatic toxicology 101(1): 13–30.
Martínez-Álvarez, R. M., A. E. Morales & A. Sanz, 2005. Antioxidant defenses in fish: biotic and abiotic factors. Reviews in Fish Biology and Fisheries 15: 75–88.
McGraw, K. J., 2005. The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Animal Behaviour 69: 757–764.
Modesto, K. A. & C. B. Martinez, 2010. Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere 78: 294–299.
Møller, A. P., C. Biard, J. D. Blount, D. C. Houston, P. Ninni, N. Saino & P. F. Surai, 2000. Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Poultry and Avian Biology Reviews 11: 137–160.
Monaghan, P., N. B. Metcalfe & R. Torres, 2009. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12: 75–92.
Mortensen, A. & L. H. Skibsted, 1996. Kinetics of parallel electron transfer from beta-carotene to phenoxyl radical and adduct formation between phenoxyl radical and beta-carotene. Free Radical Research 25: 515–523.
Mozsár, A., G. Boros, P. Sály, L. Antal & S. A. Nagy, 2015. Relationship between Fulton’s condition factor and proximate body composition in three freshwater fish species. Journal of Applied Ichthyology 31: 315–320.
Olson, V. A. & I. P. F. Owens, 1998. Costly sexual signals: are carotenoids rare, risky or required? Trends in Ecology & Evolution 13: 510–514.
Packer, L., 1992. Carotenoids. Part A, Chemistry, Separation, Quantitation, and Antioxidation. Academic Press, London, UK.
Parolini, M., A. Binelli, D. Cogni & A. Provini, 2010. Multi-biomarker approach for the evaluation of the cyto-genotoxicity of paracetamol on the zebra mussel (Dreissena polymorpha). Chemosphere 79: 489–498.
Parolini, M., C. D. Possenti, F. Karadas, G. Colombo, M. Romano, M. Caprioli, … & N. Saino, 2017. Yolk vitamin E positively affects prenatal growth but not oxidative status in yellow-legged gull embryos. Current Zoology: zox037.
Perez, C., M. Lores & A. Velando, 2008. Availability of nonpigmentary antioxidant affects red coloration in gulls. Behavioral Ecology 19: 967–973.
Perez-Rodriguez, L., 2009. Carotenoids in evolutionary ecology: re-evaluating the antioxidant role. Bioessays 31: 1116–1126.
Perez-Rodriguez, L., F. Mougeot, C. Alonso-Alvarez, J. Blas, J. Vinuela & G. R. Bortolotti, 2008. Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoris rufa). Journal of Experimental Biology 211: 2155–2161.
Peters, A., 2007. Testosterone and carotenoids: an integrated view of trade-offs between immunity and sexual signalling. Bioessays 29(5): 427–430.
Pike, T. W., J. D. Blount, J. Lindström & N. B. Metcalfe, 2007. Availability of noncarotenoid antioxidants affects the expression of a carotenoid-based sexual ornament. Biology Letters 3: 353–356.
Rahman, M. M., S. Khosravi, K. H. Chang & S. M. Lee, 2016. Effects of dietary inclusion of astaxanthin on growth, muscle pigmentation and antioxidant capacity of juvenile rainbow trout (Oncorhynchus mykiss). Preventive nutrition and food science 21(3): 281.
Robinson, M. K., R. R. Rustum, E. A. Chambers, J. D. Rounds, D. W. Wilmore & D. O. Jacobs, 1997. Starvation enhances hepatic free radical release following endotoxemia. Journal of Surgical Research 69: 325–330.
Stegen, J. C., C. M. Gienger & L. Sun, 2004. The control of color change in the Pacific tree frog, Hyla regilla. Canadian Journal of Zoology 82: 889–896.
Stephensen, C. B., 2001. Vitamin A, infection, and immune function. Annual Review of Nutrition 21(1): 167–192
Steven, D. M., 1947. Carotenoid pigmentation in trout. Nature 160: 540.
Steven, D. M., 1948. Studies on animal carotenoids. 1. Carotenoids of the brown trout (Salmo trutta Linnaeus). Journal of Experimental Biology 25: 369–387.
Stevens, M., C. A. Parraga, I. C. Cuthill, J. C. Partridge & T. S. Troscianko, 2007. Using digital photography to study animal coloration. Biological Journal of the Linnean Society 90: 211–237.
Svensson, P. A. & B. B. M. Wong, 2011. Carotenoid-based signals in behavioural ecology: a review. Behaviour 148: 131–189.
Vinkler, M. & T. Albrecht, 2010. Carotenoid maintenance handicap and the physiology of carotenoid-based signalisation of health. Naturwissenschaften 97(1): 19–28.
von Schantz, T., S. Bensch, M. Grahn, D. Hasselquist, & H. Wittzell, 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proceedings of the Royal Society of London. Series B, Biological Sciences 266: 1–12.
Wang, Y., Y. Chien & C. Pan, 2006. Effects of dietary supplementation of carotenoids on survival, growth, pigmentation, and antioxidant capacity of characins, Hyphessobrycon callistus. Aquaculture 261: 641–648.
Wedekind, C., P. Meyer, M. Frischknecht, U. A. Niggli & H. Pfander, 1998. Different carotenoids and potential information content of red coloration of male three-spined stickleback. Journal of Chemical Ecology 24: 787–801.
Wilkins, L. G., L. M. Da Cunha, L. Menin, D. Ortiz, V. Vocat-Mottier, M. Hobil, et al. 2017. Maternal allocation of carotenoids increases tolerance to bacterial infection in brown trout. Oecologia 185(3): 351–363.
Acknowledgements
We are very grateful to the Gran Paradiso National Park for the opportunity to perform this study. We would like to thank all the employers of the park surveillance involved during the sampling operations. We would like to thank Dr. Margherita Corti and Dr. Stefano Podofillini for their pivotal help in image analysis.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare to have no conflict of interest.
Additional information
Handling editor: Diego Fontaneto
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Parolini, M., Iacobuzio, R., Possenti, C.D. et al. Carotenoid-based skin coloration signals antioxidant defenses in the brown trout (Salmo trutta). Hydrobiologia 815, 267–280 (2018). https://doi.org/10.1007/s10750-018-3571-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-018-3571-6