Abstract
Carotenoids are organic pigments involved in several important physiological functions and may serve as indicators of individual quality in animals. These pigments are only obtained by animals from the diet, but they can be later transformed into other carotenoids by specific enzymatic reactions. The diet of farm-reared and probably wild red-legged partridges (Alectoris rufa) is mainly based on cereals that contain high levels of lutein and zeaxanthin. These two carotenoids are also predominant in internal tissues and blood of red-legged partridges. However, in their integuments, astaxanthin and papilioerythrinone (the last one identified in this work) are mainly present in their free form and esterified with fatty acids. According to available literature about carotenoid metabolism in animals, we propose that astaxanthin (λ max = 478 nm) and papilioerythrinone (λ max = 452–478 nm) are the result of a chromatic convergence of the transformation of dietary zeaxanthin and lutein, respectively. Moreover, the results obtained in this work provide the first identification by liquid chromatography coupled to accurate mass quadrupole time-of-flight mass spectrometer system of papilioerythrinone (m/z 581.3989 [M + H]+) in the skin (i.e., not feathers) of a vertebrate. Astaxanthin and papilioerythrinone are very close in terms of chemical structure and coloration, and the combination of these two keto-carotenoids is responsible for the red color of the ornaments in red-legged partridges.
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Alonso-Alvarez C, Galván I (2011) Free radical exposure creates paler carotenoid-based ornaments: a possible interaction in the expression of black and red traits. PLoS ONE 6:e19403
Alonso-Alvarez C, Pérez-Rodríguez L, Mateo R, Chastel O, Viñuela J (2008) The oxidation handicap hypothesis and the carotenoid allocation trade-off. J Evol Biol 21:1789–1797
Alonso-Alvarez C, Pérez-Rodríguez L, Ferrero ME, García-de Blas E, Casas F, Mougeot F (2012) Adjustment of female reproductive investment according to male carotenoid-based ornamentation in a gallinaceous bird. Behav Ecol Sociobiol 66:731–742
Arroyo B, Delibes-Mateos M, Díaz-Fernández S, Viñuela J (2012) Hunting management in relation to profitability aims: red-legged partridge hunting in central Spain. Eur J Wildl Res 58:847–855
Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558
Britton G, Liaaen-Jensen S, Pfander H (1995) Carotenoids, Volume 1B: Spectroscopy, Birkhäuser Verlag Basel Switzerland
Castillo R, Lenel R (1978) Determination and metabolism of carotenoid pigments in the hermit crab Clibanarius erythropus latreille (1818) [Syn. Cl. misanthropus heller (1863)]. Comp Biochem Physiol 59:67–73
Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S–261S
Cuthill I (2006) Color perception. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 1, Mechanisms and measurements. Havard University Press, Cambridge, pp 3–40
Díaz-Fernández S, Arroyo B, Casas F, Martínez-Haro M, Viñuela J (2013) Effect of game management on wild red-legged partridge abundance. PLoS ONE 8:e66671
Enzell CR, Back S (1995) Mass spectrometry. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, Volume 1B: Spectroscopy. Birkhäuser Verlag, Switzerland, pp 261–320
Enzell CR, Francis GW, Liaaen-Jensen S (1968) Mass spectrometric studies of carotenoids: occurrence and intensity ratios of M-92 and M-106 peaks. Acta Chem Scand 22:1054–1055
García-de Blas E, Mateo R, Viñuela J, Alonso-Alvarez C (2011) Identification of carotenoid pigments and their fatty acid esters in an avian integument combining HPLC-DAD and LC-MS analyses. J Chromatogr B 879:341–348
García-de Blas E, Mateo R, Viñuela J, Pérez-Rodríguez L, Alonso-Alvarez C (2013) Free and esterified carotenoids in ornaments of an avian species: the relationship to color expression and sources of variability. Physiol Biochem Zool 86:483–498
Goodwin TW (1984) The biochemistry of the carotenoids, Volume II: Animals. Chapman and Hall, London
Gortazar C, Villafuerte R, Martin M (2000) Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragón. Z Jagdwiss 46:23–30
Grafen A (1990) Biologiacl signals as handicaps. J Theor Biol 144:517–546
Harashima K, Ohno T, Sawachika T, Hidaka T, Ohnishi E (1972) Carotenoids in orange pupae of the swallowtail, Papilio xuthus. Insect Biochem 2:29–48
Harashima K, Nakahara J, Kato G (1976) A new ketocarotenoid in integuments of orange pupae of a swallowtail, Papilio xucthus, and carapaces of a crab, Paralithodes brevipes (Hanasakigani in Japanese). Agric Biol Chem 40:711–717
Hart NS, Vorobyev M (2005) Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191:381–392
Hill GE, Johnson JD (2012) The vitamin A–redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am Nat 180:E127–E150
LaFountain AM, Frank HA, Prum RO (2013) Carotenoids from crimson and maroon plumages of Old World orioles (Oriolidae). Arch Biochem Biophys 539:126–132
Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177
Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311
Mangoni O, Imperatore C, Tomas CR, Costantino V, Saggiomo V, Mangoni A (2011) The new carotenoid pigment moraxanthin is associated with toxic microalgae. Mar Drugs 9:242–255
Maoka T (2009) Recent progress in structural studies of carotenoids in animals and plants. Arch Biochem Biophys 483:191–195
Maoka T (2011) Carotenoids in marine animals. Mar Drugs 9:278–293
Matsuno T, Maoka T (1988) The carotenoids of crab Paralithodes brevipes (Hanasakigani in Japanese). Nippon Suisan Gakkaishi 54:1437–1442
Matsuno T, Ookubo M (1982) The first isolation and identification of fritschiellaxanthin from a crab Sesarma haematocheir (AKATEGANI in Japanese). B Jpn Soc Sci Fish 48:653–659
McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 1, Mechanisms and measurements. Harvard University Press, Cambridge, pp 177–242
McGraw KJ, Gregory AJ (2004) Carotenoid pigments in male American goldfinches: what is the optimal biochemical strategy for becoming colourful? Biol J Linn Soc 83:273–280
McGraw KJ, Hardy LSJ (2006) Astaxanthin is responsible for the pink plumage flush in Franklin’s and Ring-billed gulls. Field Ornithol 77:29–33
Miller NJ, Sampson J, Candeias LP, Bramley PM, Rice-Evans CA (1996) Antioxidant activities of carotenes and xanthophylls. FEBS Lett 384:240–242
Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, inmmunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159
Murillo E, McLean R, Britton G, Agócs A, Nagy V, Deli J (2011) Sapotexanthin, an A-provitamin carotenoid from Red Mamey (Pouteria sapota). J Nat Prod 74:283–385
Pérez-Bonilla A, Frikha M, Mirzaie S, García J, Mateos GG (2011) Effects of the main cereal and type of fat of the diet on productive performance and egg quality of brown-egg laying hens from 22 to 54 weeks of age. Poult Sci 90:2801–2810
Pérez-Rodriguez L (2009) Carotenoids in evolutionary ecology: re-evaluating the antioxidant role. BioEssays 31:1116–1126
Pérez-Rodriguez L, Viñuela J (2008) Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged-partridge (Alectoris rufa). Naturwissenschaften 95:821–830
Rodríguez-Estival J, Martínez-Haro M, Martín-Hernando MP, Mateo R (2010) Sub-chronic effects of nitrate in drinking water on red-legged partridge (Alectoris rufa): Oxidative stress and T-cell mediated immune function. Environ Res 110:169–175
Stahl W, Sies H (2003) Antioxidant activity of carotenoids. Mol Asp Med 24:345–351
Stradi R (1998) The color of flight: carotenoids in bird plumage. Gruppo Editoriale Informatico Solei, Milan
Stradi R, Pini E, Celentano G (2001) Carotenoids in bird plumage: the complement of red pigments in the plumage of wild and captive bullfinch (Pyrrhula pyrrhula). Comp Biochem Physiol B 128:529–535
Suhnel S, Lagreze F, Ferreira JF, Campestrini LH, Maraschin M (2009) Carotenoid extraction from the gonad of the scallop Nodipecten nodosus (Linnaeus, 1758) (Bivalvia: Pectinidae). Braz J Biol 69:209–215
Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham
Zahavi A (1975) Mate selection — a selection for a handicap. J Theor Biol 53:205–214
Acknowledgments
We thank Akira Yamanaka (Department of Biology and Chemistry, Yamaguchi University, Japan) and Sayuri Shigematsu (Department of Microbiology and Immunology, Nagasaki University, Japan) for providing samples of swallowtail and crab, and Estación Biológica de Doñana (CSIC, Sevilla, Spain) and the Museo Nacional de Ciencias Naturales (CSIC, Madrid, Spain) for providing bullfinch feathers. We also thank the owners and managers of the farms and wild areas that supplied partridges. Javier Viñuela provided useful ideas in the first stages of the study. We also appreciate the help of Antonio Pérez-Gálvez with the MS/MS data, and James D. Johnson and another one anonymous reviewer for constructive comments on the manuscript. Esther García-de Blas was supported by a predoctoral grant (JAE-PRE) from the Consejo Superior de Investigaciones Científicas (CSIC) cofinanced by Fondo Social Europeo. This study was funded by Consejería de Educación y Ciencia, Junta de Comunidades de Castilla la Mancha (PII1I09-0271-5037), and Ministerio de Economía y Competitividad (CGL2009-10883-C02-02 and CGL2012-40229-C02-01) from the Spanish government.
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García-de Blas, E., Mateo, R., Guzmán Bernardo, F.J. et al. Astaxanthin and papilioerythrinone in the skin of birds: a chromatic convergence of two metabolic routes with different precursors?. Naturwissenschaften 101, 407–416 (2014). https://doi.org/10.1007/s00114-014-1169-z
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DOI: https://doi.org/10.1007/s00114-014-1169-z