Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Bernhard K, Grosjean M (1995) Infrared spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhauser Verlag, Basel, pp 117–134

    Google Scholar 

  • Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhäuser Verlag, Basel, pp 13–62

    Google Scholar 

  • 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 69:2075–2084

    Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (2004) In: Carotenoids handbook. Birkhäuser Verlag, Basel

  • 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 62:2817–2824

    Article  CAS  Google Scholar 

  • 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 117:11209–11219

    Article  CAS  PubMed  Google Scholar 

  • Curry B, Palings I, Broek A, Pardoen JA, Mulder PPJ, Lugtenburg J et al (1984) Vibrational analysis of 13-cis-retinal. J Phys Chem 88:688–702

    Article  CAS  Google Scholar 

  • Englert G (1995) NMR spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B spectroscopy. Birkhauser, Basel, pp 147–259

    Google Scholar 

  • Enzell CR, Back S (1995) Mass spectrometry. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhauser, Basel, pp 261–317

    Google Scholar 

  • 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 71–80

    Google Scholar 

  • 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 21:384–393

    Article  CAS  PubMed  Google Scholar 

  • Gottlieb HE, Kotlyar V, Nudelman A (1997) NMR chemical shifts of common laboratory solvents as trace impurities. J Org Chem 62:7512–7515

    Article  CAS  PubMed  Google Scholar 

  • 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 320:1763–1768

    Article  CAS  PubMed  Google Scholar 

  • Hudon J (1991a) Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can J Zool 69:2320–23111

    Article  Google Scholar 

  • Hudon J (1991b) Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can J Zool 69:2311–2320

    Article  CAS  Google Scholar 

  • 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 76:776–790

    Article  CAS  PubMed  Google Scholar 

  • 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 109:3120–3127

    Article  CAS  PubMed  Google Scholar 

  • 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 35:567–580

    Article  Google Scholar 

  • Vetter W, Englert G, Rigassi N, Schwieter U (1971) Spectroscopic methods. In: Isler O (ed) Carotenoids. Birkhäuser Verlag, Basel, pp 189–266

  • Koyama Y (1995) Resonance Raman spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: spectroscopy. Birkhäuser Verlag, Basel, pp 135–146

    Google Scholar 

  • 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 161–188

    Chapter  Google Scholar 

  • 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 327–408

  • 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 19:37–49

    Article  CAS  Google Scholar 

  • 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 1544:301–310

    Article  CAS  PubMed  Google Scholar 

  • 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 504:142–153

    Article  CAS  PubMed  Google Scholar 

  • 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 177–242

    Google Scholar 

  • 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 243–294

    Google Scholar 

  • 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 74:843–852

    Article  CAS  PubMed  Google Scholar 

  • 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 57:391–397

    Article  Google Scholar 

  • 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 9:3338–3350

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merlin JC (1987) Resonance Raman analysis of astaxanthin–protein complexes. J Raman Spectrosc 18:519–523

    Article  CAS  Google Scholar 

  • Mori Y, Yamano K, Hashimoto H (1996) Bistable aggregate of all-trans-astaxanthin in an aqueous solution. Chem Phys Lett 254:84–88

    Article  CAS  Google Scholar 

  • 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 3544:1–22

    Article  Google Scholar 

  • 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 115:3216–3225

    Article  CAS  PubMed  Google Scholar 

  • 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 154:373–380

    Article  PubMed  Google Scholar 

  • 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 182:1095–1116

    Article  CAS  PubMed  Google Scholar 

  • 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 182:1095–1116

    Article  CAS  PubMed  Google Scholar 

  • Rimai L, Heyde ME, Gill D (1973) Vibrational spectra of some carotenoids and related linear polyenes. A Raman spectroscopic study. J Am Chem Soc 95:4493–4501

    Article  CAS  PubMed  Google Scholar 

  • 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 189–201

    Google Scholar 

  • Robert B (2009) Resonance Raman spectroscopy. Photosynth Res 101:147–155

    Article  CAS  PubMed  Google Scholar 

  • 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 14:299–309

    Article  CAS  Google Scholar 

  • Salares VR, Young NM, Carey PR, Bernstein HJ (1977) Excited state (exciton) interactions in polyene aggregates. J Raman Spectrosc 6:282–288

    Article  CAS  Google Scholar 

  • 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 576:176–191

    Article  CAS  PubMed  Google Scholar 

  • 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 9:2563–2580

    Google Scholar 

  • 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 94:4161–4170

    Article  CAS  Google Scholar 

  • 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 81–107

  • Stoddard MC, Prum RO (2011) How colorful are birds? Evolution of the avian plumage color gamut. Behav Ecol 22:1042–1052

    Article  Google Scholar 

  • 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 117–146

    Google Scholar 

  • 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 670:337–348

    Article  CAS  Google Scholar 

  • 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:131–143

    Article  CAS  Google Scholar 

  • 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:427–432

    Article  CAS  Google Scholar 

  • 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:85–91

    Article  CAS  Google Scholar 

  • 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 120:223–230

    Article  Google Scholar 

  • 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 113:5311–5317

    Article  CAS  PubMed  Google Scholar 

  • van Breemen RB, Dong L, Pajkovic ND (2012) Atmospheric pressure chemical ionization tandem mass spectrometry of carotenoids. Int J Mass Spectrom 312:163–172

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 127:1438–1445

    Article  PubMed  Google Scholar 

  • Veronelli M, Zerbi G, Stradi R (1995) In-situ resonance Raman-spectra of carotenoids in birds feathers. J Raman Spectrosc 26:683–692

    Article  CAS  Google Scholar 

  • 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 116:10617–10630

    Article  CAS  PubMed  Google Scholar 

  • 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 5:358–370

    Article  CAS  PubMed  Google Scholar 

  • Weesie RJ, Merlin JC, Lugtenberg J, Britton G, Jansen FJ, Cornard JP (1999b) Semiempirical and Raman spectroscopic studies of carotenoids. Biospectroscopy 5:19–33

    Article  CAS  PubMed  Google Scholar 

  • 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 216–247

  • Zagalsky PF (1995) Carotenoproteins. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1A. Birkhauser, Basel, pp 287–294

    Google Scholar 

  • 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 D59:1529–1531

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. George Britton for helpful discussions. Work in the laboratory of H.A.F. was supported by the University of Connecticut Research Foundation. Work by R.O.P was supported by the W.R. Coe Fund of Yale University. Work in the laboratory of M.J.T was supported by the National Science Foundation (under CHE-1057198), and UCSD start-up support. We thank Kristof Zyskowski and the Yale Peabody Museum of Natural History for access to broadbill feather specimens used in this study. We thank Kristof Zyskowski, Bjorn Oleson, and VIREO/Spike Baker for permission to reproduce their photos of broadbills in Fig. 2.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology and Peabody Museum of Natural History, Yale University, 21 Sachem Street, New Haven, CT, 06511, USA

    Richard O. Prum

  2. Department of Chemistry, University of Connecticut, 55 North Eagleville Road, Storrs, CT, 06269, USA

    Amy M. LaFountain & Harry A. Frank

  3. Department of Chemistry, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA

    Christopher J. Berg & Michael J. Tauber

Authors
  1. Richard O. Prum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy M. LaFountain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher J. Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael J. Tauber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Harry A. Frank
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard O. Prum.

Additional information

Communicated by G. Heldmaier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1787 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prum, R.O., LaFountain, A.M., Berg, C.J. et al. Mechanism of carotenoid coloration in the brightly colored plumages of broadbills (Eurylaimidae). J Comp Physiol B 184, 651–672 (2014). https://doi.org/10.1007/s00360-014-0816-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-014-0816-1

Keywords

Search

Navigation