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

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 184, Issue 5, 2014, Pages 651-672

  Prum, Richard O ^a   LaFountain, Amy M ^b   Berg, Christopher J ^c   Tauber, Michael J ^c   Frank, Harry A ^b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

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

Indexed keywords

CALYPTOMENA VIRIDIS; CYMBIRHYNCHUS; CYMBIRHYNCHUS MACRORHYNCHOS; EURYLAIMIDAE; EURYLAIMUS; EURYLAIMUS JAVANICUS; EURYLAIMUS OCHROMALUS; MYIAGRA; PICIDAE; PICINAE; PSARISOMUS DALHOUSIAE;

CAROTENOID;

ANIMAL; COLOR; FEATHER; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RAMAN SPECTROMETRY; SONGBIRD; TANDEM MASS SPECTROMETRY;

ANIMALS; CAROTENOIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLOR; FEATHERS; FEMALE; MAGNETIC RESONANCE SPECTROSCOPY; MALE; PASSERIFORMES; SPECTRUM ANALYSIS, RAMAN; TANDEM MASS SPECTROMETRY;

EID: 84903155671     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-014-0816-1     Document Type: Article

References (63)

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 117-134.
2. Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: Spectroscopy. Birkhäuser Verlag, Basel, pp 13-62.
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: 2075-2084.
4. Britton G, Liaaen-Jensen S, Pfander H (2004) In: Carotenoids handbook. Birkhäuser Verlag, Basel.
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: 2817-2824.
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: 11209-11219.
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: 688-702.
8. Englert G (1995) NMR spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B spectroscopy. Birkhauser, Basel, pp 147-259.
9. Enzell CR, Back S (1995) Mass spectrometry. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: Spectroscopy. Birkhauser, Basel, pp 261-317.
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 71-80.
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: 384-393.
12. Gottlieb HE, Kotlyar V, Nudelman A (1997) NMR chemical shifts of common laboratory solvents as trace impurities. J Org Chem 62: 7512-7515.
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: 1763-1768.
14. Hudon J (1991a) Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can J Zool 69: 2320-23111.
15. Hudon J (1991b) Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can J Zool 69: 2311-2320.
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: 776-790.
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: 3120-3127.
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: 567-580.
19. Vetter W, Englert G, Rigassi N, Schwieter U (1971) Spectroscopic methods. In: Isler O (ed) Carotenoids. Birkhäuser Verlag, Basel, pp 189-266.
20. Koyama Y (1995) Resonance Raman spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids vol 1B: Spectroscopy. Birkhäuser Verlag, Basel, pp 135-146.
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 161-188.
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 327-408.
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: 37-49.
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: 301-310.
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: 142-153.
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 177-242.
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 243-294.
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: 843-852.
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: 391-397.
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: 3338-3350.
31. Merlin JC (1987) Resonance Raman analysis of astaxanthin-protein complexes. J Raman Spectrosc 18: 519-523.
32. Mori Y, Yamano K, Hashimoto H (1996) Bistable aggregate of all-trans-astaxanthin in an aqueous solution. Chem Phys Lett 254: 84-88.
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: 1-22.
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: 3216-3225.
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: 373-380.
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: 1095-1116.
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: 1095-1116.
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: 4493-4501.
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 189-201.
40. Robert B (2009) Resonance Raman spectroscopy. Photosynth Res 101: 147-155.
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: 299-309.
42. Salares VR, Young NM, Carey PR, Bernstein HJ (1977) Excited state (exciton) interactions in polyene aggregates. J Raman Spectrosc 6: 282-288.
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: 176-191.
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: 2563-2580.
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: 4161-4170.
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 81-107.
47. Stoddard MC, Prum RO (2011) How colorful are birds? Evolution of the avian plumage color gamut. Behav Ecol 22: 1042-1052.
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 117-146.
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: 337-348.
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: 131-143.
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: 427-432.
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: 85-91.
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: 223-230.
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: 5311-5317.
55. van Breemen RB, Dong L, Pajkovic ND (2012) Atmospheric pressure chemical ionization tandem mass spectrometry of carotenoids. Int J Mass Spectrom 312: 163-172.
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: 1438-1445.
57. Veronelli M, Zerbi G, Stradi R (1995) In-situ resonance Raman-spectra of carotenoids in birds feathers. J Raman Spectrosc 26: 683-692.
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: 10617-10630.
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: 358-370.
60. Weesie RJ, Merlin JC, Lugtenberg J, Britton G, Jansen FJ, Cornard JP (1999b) Semiempirical and Raman spectroscopic studies of carotenoids. Biospectroscopy 5: 19-33.
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 216-247.
62. Zagalsky PF (1995) Carotenoproteins. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1A. Birkhauser, Basel, pp 287-294.
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: 1529-1531.