Journal of Comparative Physiology B

, Volume 184, Issue 5, pp 651–672 | Cite as

Mechanism of carotenoid coloration in the brightly colored plumages of broadbills (Eurylaimidae)

  • Richard O. Prum
  • Amy M. LaFountain
  • Christopher J. Berg
  • Michael J. Tauber
  • Harry A. Frank
Original Paper

Abstract

The plumage carotenoids of six species from five genera of broadbills (Eurylaimidae) have been examined. These plumages are crimson, violet, purple-maroon, or yellow. Two genera also have brilliant green plumages that are produced by a combination of structural coloration and unknown carotenoids. Six different carotenoids from nine different plumage patches were identified, including two previously unknown molecules, using high-performance liquid chromatography, mass spectrometry, and MS/MS fragment analysis. The yellow pigment in Eurylaimus javanicus and Eurylaimus ochromalus is identified as the novel carotenoid, 7,8-dihydro-3′-dehydro-lutein. The yellow and green plumages of Psarisomus dalhousiae contain the unmodified dietary carotenoids lutein and zeaxanthin. The brilliant green feathers of Calyptomena viridis contain a mixture of lutein and two other xanthophylls that have previously been found only in woodpeckers (Picinae). The crimson and violet colors of Cymbirhynchus, Sarcophanops, and Eurylaimus are produced by a novel pigment, which is identified as 2,3-didehydro-papilioerythrinone. The molecular structure of this carotenoid was confirmed using 1H nuclear magnetic resonance, correlated two-dimensional spectroscopy, and two-dimensional nuclear Overhauser effect spectroscopy. Resonance Raman (rR) spectroscopy carried out at room and low temperatures was used to probe the configuration and conformation of 2,3-didehydro-papilioerythrinone in situ within crimson C. macrorhynchos and purple-red E. javanicus feathers. The rR spectra reveal that the pigment is in an all-trans configuration and appears to be relatively planar in the feathers. The likely metabolic pathways for the production of broadbill carotenoids from dietary precursors are discussed.

Keywords

Carotenoid metabolism Feather coloration High-performance liquid chromatography Nuclear magnetic resonance Pigment analysis Resonance Raman spectroscopy 

Supplementary material

360_2014_816_MOESM1_ESM.docx (1.7 mb)
Supplementary material 1 (DOCX 1787 kb)

References

  1. Bernhard K, Grosjean M (1995) Infrared spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhauser Verlag, Basel, pp 117–134Google Scholar
  2. Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhäuser Verlag, Basel, pp 13–62Google Scholar
  3. Britton G, Weesie RJ, Askin D, Warburton JD, Gallardo-Guerrero L, Jansen FJ, de Groot HJM, Lugtenburg J, Cornard J-P, Merlin J-C (1997) Carotenoid blues: structural studies on carotenoproteins. Pure Appl Chem 69:2075–2084Google Scholar
  4. Britton G, Liaaen-Jensen S, Pfander H (2004) In: Carotenoids handbook. Birkhäuser Verlag, BaselGoogle Scholar
  5. Buchecker R, Eugster CH (1979) Eine Suche nach 3′-Epilutein (=(3R,3′S,6′R)-β, ε-Carotin-3,3′-diol) und 3′, O-Didehydrolutein (=(3R, 6′R)-3-Hydroxy-β, ε-carotin-3′-on) in Eigelb, in Blüten von Caltha palustris und in Herbstblättern. Helv Chim Acta 62:2817–2824CrossRefGoogle Scholar
  6. Christensson N, Židek K, Magdaong NCM, LaFountain AM, Frank HA, Zigmantas D (2013) Origin of the bathochromic shift of astaxanthin in lobster protein: 2D electronic spectroscopy investigation of β-crustacyanin. J Phys Chem B 117:11209–11219PubMedCrossRefGoogle Scholar
  7. Curry B, Palings I, Broek A, Pardoen JA, Mulder PPJ, Lugtenburg J et al (1984) Vibrational analysis of 13-cis-retinal. J Phys Chem 88:688–702CrossRefGoogle Scholar
  8. Englert G (1995) NMR spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B spectroscopy. Birkhauser, Basel, pp 147–259Google Scholar
  9. Enzell CR, Back S (1995) Mass spectrometry. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhauser, Basel, pp 261–317Google Scholar
  10. Eugster CH (1995) Chemical derivatization: microscale tests for the presence of common functional groups in carotenoids. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1A: isolation and analysis. Birkhäuser Verlag, Basel, pp 71–80Google Scholar
  11. Eyring G, Curry B, Broek A, Lugtenburg J, Mathies R (1982) Assignment and interpretation of hydrogen out-of-plane vibrations in the resonance Raman spectra of rhodopsin and bathorhodopsin. Biochemistry 21:384–393PubMedCrossRefGoogle Scholar
  12. Gottlieb HE, Kotlyar V, Nudelman A (1997) NMR chemical shifts of common laboratory solvents as trace impurities. J Org Chem 62:7512–7515PubMedCrossRefGoogle Scholar
  13. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768PubMedCrossRefGoogle Scholar
  14. Hudon J (1991a) Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can J Zool 69:2320–23111CrossRefGoogle Scholar
  15. Hudon J (1991b) Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can J Zool 69:2311–2320CrossRefGoogle Scholar
  16. Hudon J, Grether GF, Millie DF (2003) Marginal differentiation between the sexual and general carotenoid pigmentation of guppies (Poecilia reticulata) and a possible visual explanation. Physiol Biochem Zool 76:776–790PubMedCrossRefGoogle Scholar
  17. Ilagan RP, Christensen RL, Chapp TW, Gibson GN, Pascher T, Polivka T et al (2005) Femtosecond time-resolved absorption spectroscopy of astaxanthin in solution and in α-crustacyanin. J Phys Chem A 109:3120–3127PubMedCrossRefGoogle Scholar
  18. Irestedt M, Ohlson JI, Zuccon D, Källersjö M, Ericson PGP (2006) Nuclear DNA from old collections of avian study skins reveals the evolutionary history of the Old World suboscines (Aves, Passeriformes). Zoolog Scr 35:567–580CrossRefGoogle Scholar
  19. Vetter W, Englert G, Rigassi N, Schwieter U (1971) Spectroscopic methods. In: Isler O (ed) Carotenoids. Birkhäuser Verlag, Basel, pp 189–266Google Scholar
  20. Koyama Y (1995) Resonance Raman spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhäuser Verlag, Basel, pp 135–146Google Scholar
  21. Koyama Y, Fujii R (1999) Cis-trans carotenoids in photosynthesis: configurations, excited-state properties and physiological functions. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The photochemistry of carotenoids, vol 8. Kluwer Academic Publishers, Dordrecht, pp 161–188CrossRefGoogle Scholar
  22. Koyama Y, Hashimoto H (1993) Spectroscopic studies of carotenoids in photosynthetic systems. In: Young AJ, Britton G (eds) Carotenoids in photosynthesis. Chapman and Hall, London, pp 327–408Google Scholar
  23. Koyama Y, Takatsuka I, Nakata M, Tasumi M (1988) Raman and infrared spectra of the all-trans, 7-cis, 9-cis, 13-cis and 15-cis isomers of b-carotene: key bands distinguishing stretched or terminal-bent configurations from central-bent configurations. J Raman Spectrosc 19:37–49CrossRefGoogle Scholar
  24. Krawczyk S, Britton G (2001) A study of protein-carotenoid interactions in the astxanthin-protein crustacyanin by absorption and Stark spectroscopy; evidence for the presence of three spectrally distinct species. Biochim Biophys Acta 1544:301–310PubMedCrossRefGoogle Scholar
  25. LaFountain AM, Kaligotla S, Cawley S, Riedl KM, Schwartz SJ, Frank HA et al (2010) Novel methoxy-carotenoids from the burgundy-colored plumage of the Pompadour Cotinga Xipholena punicea. Arch Biochem Biophys 504:142–153PubMedCrossRefGoogle Scholar
  26. McGraw KJ (2006a) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration vol 1: mechanisms and measurements. Harvard University Press, Cambridge, pp 177–242Google Scholar
  27. McGraw KJ (2006b) Mechanics of melanin-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration vol 1: mechanisms and measurements. Harvard University Press, Cambridge, pp 243–294Google Scholar
  28. McGraw KJ, Hill GE, Stradi R, Parker RS (2001) The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in the male American goldfinches (Carduelis tristis) and Northern cardinal (Cadinalis cardinalis). Physiol Biochem Zool 74:843–852PubMedCrossRefGoogle Scholar
  29. McGraw KJ, Hudon J, Hill GE, Parker RS (2005) A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behav Ecol Sociobiol 57:391–397CrossRefGoogle Scholar
  30. Mendes-Pinto MM, LaFountain AM, Stoddard MC, Prum RO, Frank HA, Robert B (2012) Variation in carotenoid-protein interactions by bird feather proteins produces novel plumage coloration. J R Soc Interface 9:3338–3350PubMedCentralPubMedCrossRefGoogle Scholar
  31. Merlin JC (1987) Resonance Raman analysis of astaxanthin–protein complexes. J Raman Spectrosc 18:519–523CrossRefGoogle Scholar
  32. Mori Y, Yamano K, Hashimoto H (1996) Bistable aggregate of all-trans-astaxanthin in an aqueous solution. Chem Phys Lett 254:84–88CrossRefGoogle Scholar
  33. Moyle RG, Chesser RT, Prum RO, Schikler P, Cracraft J (2006) Phylogeny and evolutionary history of old world suboscine birds (Aves: Eurylaimides). Am Mus Novit 3544:1–22CrossRefGoogle Scholar
  34. Neugebauer J, Veldstra J, Buda F (2011) Theoretical spectroscopy of astaxanthin in crustacyanin proteins: absorption, circular dichroism, and nuclear magnetic resonance. J Phys Chem B 115:3216–3225PubMedCrossRefGoogle Scholar
  35. Prager M, Johansson EIA, Andersson S (2009) Differential ability of carotenoid C4-oxygenation in yellow and red bishop species (Euplectes spp.). Comp Biochem Physiol B 154:373–380PubMedCrossRefGoogle Scholar
  36. Prum RO, LaFountain AM, Berro J, Stoddard MC, Frank HA (2012a) Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae). J Comp Physiol B 182:1095–1116PubMedCrossRefGoogle Scholar
  37. Prum RO, LaFountain AM, Berro J, Stoddard MC, Frank HA (2012b) Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae). J Comp Physiol B 182:1095–1116PubMedCrossRefGoogle Scholar
  38. Rimai L, Heyde ME, Gill D (1973) Vibrational spectra of some carotenoids and related linear polyenes. A Raman spectroscopic study. J Am Chem Soc 95:4493–4501PubMedCrossRefGoogle Scholar
  39. Robert B (1999) The electronic structure, stereochemistry and resonance Raman spectroscopy of carotenoids. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) Advances in photosynthesis, vol 8. Kluwer Academic Publishers, Dordrecht, pp 189–201Google Scholar
  40. Robert B (2009) Resonance Raman spectroscopy. Photosynth Res 101:147–155PubMedCrossRefGoogle Scholar
  41. Saito S, Tasumi M, Eugster CH (1983) Resonance Raman-spectra (5800-40 CM-1) of all-trans and 15-cis isomers of beta-carotene in the solid-state and in solution-measurements with various laser lines from ultraviolet to red. J Raman Spectrosc 14:299–309CrossRefGoogle Scholar
  42. Salares VR, Young NM, Carey PR, Bernstein HJ (1977) Excited state (exciton) interactions in polyene aggregates. J Raman Spectrosc 6:282–288CrossRefGoogle Scholar
  43. Salares VR, Young NM, Bernstein HJ, Carey PR (1979) Mechanisms of spectral shifts in lobster carotenoproteins—the resonance Raman spectra of ovoverdin and the crustacyanins. Biochim Biophys Acta 576:176–191PubMedCrossRefGoogle Scholar
  44. Saranathan V, Forster JD, Noh H, Liew SF, Mochrie SGJ, Cao H et al (2012) Structure and optical function of amorphous photonic nanostructures from avian feather barbs: a comparative small angle X-ray scattering (SAXS) analysis of 229 bird species. J R Soc Interface 9:2563–2580Google Scholar
  45. Schaffer HE, Chance RR, Silbey RJ, Knoll K, Schrock RR (1991) Conjugation length dependence of Raman scattering in a series of linear polyenes: implications for polyacetylene. J Chem Phys 94:4161–4170CrossRefGoogle Scholar
  46. Schiedt K, Liaaen-Jensen S (1995) Isolation and analysis. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1A: isolation and analysis. Birkhäuser Verlag, Basel, pp 81–107Google Scholar
  47. Stoddard MC, Prum RO (2011) How colorful are birds? Evolution of the avian plumage color gamut. Behav Ecol 22:1042–1052CrossRefGoogle Scholar
  48. Stradi R (1999) Pigmenti e sistematica degli uccelli. In: Brambilla L, Canali G, Mannucci E, Massa R, Saino N, Stradi R, Zerbi G (eds) Colori in volo: il piumaggio degli ucceli. Universita degli Studi di Milano, Milan, pp 117–146Google Scholar
  49. Stradi R, Celentano G, Nava D (1995a) Separation and identification of carotenoids in bird’s plumage by high-performance liquid chromatography-diode-array detection. J Chromatogr B 670:337–348CrossRefGoogle Scholar
  50. Stradi R, Celentano G, Rossi E, Rovati G, Pastore M (1995b) Carotenoids in bird plumage: the carotenoid pattern in a series of Paleartic Carduelinae. Comp Biochem Physiol 110B:131–143CrossRefGoogle Scholar
  51. Stradi R, Rossi E, Celentano G, Bellardi B (1996) Carotenoids in bird plumage: the pattern in three Loxia species and in Pinicola enucleator. Comp Biochem Physiol 113B:427–432CrossRefGoogle Scholar
  52. Stradi R, Celentano G, Boles M, Mercato F (1997) Carotenoids in bird plumage: the pattern in a series of red-pigmented Carduelinae. Comp Biochem Physiol 117B:85–91CrossRefGoogle Scholar
  53. Stradi R, Hudon J, Celentano G, Pini E (1998) Carotenoids in bird plumage: the complement of yellow and red pigments in true woodpeckers (Picinae). Comp Biochem Physiol B: Biochem Mol Biol 120:223–230CrossRefGoogle Scholar
  54. Strambi A, Durbeej B (2009) Excited-state modeling of the astaxanthin dimer predicts a minor contribution from exciton coupling to the bathochromic shift in crustacyanin. J Phys Chem B 113:5311–5317PubMedCrossRefGoogle Scholar
  55. van Breemen RB, Dong L, Pajkovic ND (2012) Atmospheric pressure chemical ionization tandem mass spectrometry of carotenoids. Int J Mass Spectrom 312:163–172PubMedCentralPubMedCrossRefGoogle Scholar
  56. van Wijk AA, Spaans A, Uzunbajakava N, Otto C, de Groot HJ, Lugtenburg J et al (2005) Spectroscopy and quantum chemical modeling reveal a predominant contribution of excitonic interactions to the bathochromic shift in alpha-crustacyanin, the blue carotenoprotein in the carapace of the lobster Homarus gammarus. J Am Chem Soc 127:1438–1445PubMedCrossRefGoogle Scholar
  57. Veronelli M, Zerbi G, Stradi R (1995) In-situ resonance Raman-spectra of carotenoids in birds feathers. J Raman Spectrosc 26:683–692CrossRefGoogle Scholar
  58. Wang C, Berg CJ, Hsu C-C, Merrill BA, Tauber MJ (2012) Characterization of carotenoid aggregates by steady-state optical spectroscopy. J Phys Chem B 116:10617–10630PubMedCrossRefGoogle Scholar
  59. Weesie RJ, Merlin JC, De Groot HJM, Britton G, Lugtenberg J, Jansen FJ et al (1999a) Resonance Raman spectroscopy and quantum chemical modeling studies of protein-astaxanthin interactions in a-crustacyanin (major blue carotenoprotein complex in carapace of lobster, Homarus gammarus). Biospectroscopy 5:358–370PubMedCrossRefGoogle Scholar
  60. Weesie RJ, Merlin JC, Lugtenberg J, Britton G, Jansen FJ, Cornard JP (1999b) Semiempirical and Raman spectroscopic studies of carotenoids. Biospectroscopy 5:19–33PubMedCrossRefGoogle Scholar
  61. Zagalsky PF (1985) Invertebrate carotenoproteins. In: Law JH, Rilling HC (eds) Methods in enzymology, vol III: steroids and isoprenoids part B. Academic Press, New York, pp 216–247Google Scholar
  62. Zagalsky PF (1995) Carotenoproteins. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1A. Birkhauser, Basel, pp 287–294Google Scholar
  63. Zagalsky PF (2003) β-Crustacyanin, the blue-purple carotenoprotein of lobster carapace: consideration of the bathochromic shift of the protein-bound astaxanthin. Acta Crystallogr D D59:1529–1531CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Richard O. Prum
    • 1
  • Amy M. LaFountain
    • 2
  • Christopher J. Berg
    • 3
  • Michael J. Tauber
    • 3
  • Harry A. Frank
    • 2
  1. 1.Department of Ecology and Evolutionary Biology and Peabody Museum of Natural HistoryYale UniversityNew HavenUSA
  2. 2.Department of ChemistryUniversity of ConnecticutStorrsUSA
  3. 3.Department of ChemistryUniversity of California, San DiegoLa JollaUSA

Personalised recommendations