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Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays

Richard O. Prum^1,* and Rodolfo Torres²

¹ Department of Ecology and Evolutionary Biology, and Natural History Museum, Dyche Hall, University of Kansas, Lawrence, KS 66045-7561, USA
² Department of Mathematics, University of Kansas, Lawrence, KS 66045-2142, USA

View larger version (11K): [in a new window]   Fig. 1. Comparison of incoherent and coherent scattering mechanisms of biological structural colour production. (A) Incoherent scattering is differential scattering of wavelengths by individual light-scattering objects. In Rayleigh (also known as Tyndall) scattering, smaller wavelengths are preferentially scattered. The phase relationships among light waves scattered from different objects are ignored and assumed to be random. (B) Coherent scattering is differential interference or reinforcement of wavelengths scattered by multiple light-scattering objects (x, y). Coherent scattering of specific wavelengths is determined by the phase relationships among the scattered waves. Scattered wavelengths that are out of phase will cancel each other out, but scattered wavelengths that are in phase will be constructively reinforced and coherently scattered. Phase relationships of wavelengths scattered by two different objects (x, y) are given by the differences in the path lengths of light scattered by the first object (x: 1–1') and a second object (y: 2–2') as measured from planes perpendicular to the incident (a) and reflected (b) waves in the mean refractive index of the media.

View larger version (135K): [in a new window]   Fig. 2. Structurally coloured ornaments of a sample of the non-passeriform birds examined: (A) Dromaius novaehollandiae, (B) Oxyura jamaicensis, (C) Numida meleagris, (D) Lophura bulweri, (E) Tragopan temminckii, (F) Tragopan caboti, (G) Syrigma sibalatrix, (H) Pilherodius pileatus and (I) Opisthocomus hoazin. A, reproduced with permission from Nate Rice; B,D–F, reproduced with permission from Kenneth Fink; C,H,I, reproduced with permission from VIREO; G, reproduced with permission from Roger Boyd.

View larger version (86K): [in a new window]   Fig. 3. Structurally coloured ornaments of a sample of the piciform and passeriform birds examined: (A) Selenidera reinwardtii, (B) Ramphastos vitellinus, (C) Ramphastos toco, (D) Neodrepanis coruscans, (E) Philepitta castanea, (F) Myrmeciza ferruginea, (G) Gymnopithys leucapsis, (H) Procnias alba, (I) Perissocephalus tricolor, (J) Dyaphorophyia concreta, (K) Terpsiphone mutata and (L) Leucopsar rothschildi. A,F–J, reproduced with permission from VIREO; B,C,L, reproduced with permission from Kenneth Fink; H, reproduced with permission from Nate Rice; D, reproduced with permission from Steve Zack; K, reproduced with permission from Tom Schulenberg.

View larger version (44K): [in a new window]   Fig. 4. Reflectance spectra of structurally coloured avian ornaments: (A) Oxyura jamaicensis, light blue; (B) Lophura bulweri, dark blue; (C) Lophophorus impejanus, dark blue; (D) Tragopan temminckii, dark blue; (E) Tragopan temminckii, light blue; (F) Tragopan caboti, orange; (G) Syrigma sibilatrix, light blue; (H) Ramphastos toco, dark blue and (I) Dyaphorophyia concreta, yellow-green.

View larger version (125K): [in a new window]   Fig. 5. Light micrographs of structurally coloured, white and pigmented bird skin: (A) Chaemapetes unicolor, dark blue; (B) Numida meleagris, dark blue; (C) Tragopan temminckii, light blue; (D) Opisthocomus hoazin, dark blue; (E) Ramphastos vitellinus, dark blue; (F) Selenidera reinwardtii, green; (G) Procnias nudicollis, white leg skin; (H) Procnias nudicollis, structurally green throat skin and (I) Tragopan temminckii, red, lateral lappet patches. All specimens stained with Masson's trichrome, which stains collagen blue and cells red. All scale bars represent 100 µm, except in C, which represents 50 µm. Abbreviations: c, collagen macrofibrils; cc, collagenocytes; cp, capillaries; e, epidermis; m, melanosomes.

View larger version (156K): [in a new window]   Fig. 6. Transmission electron micrographs of structurally coloured and carotenoid pigmented bird skin. Collagen macrofibrils of (A,B) Tragopan satyra and (C) Tragopan caboti. Lipid-filled pigment cells immediately under the epidermis in (D) Dyaphorophyia concreta yellowish green, (E) Tragopan caboti orange and (F) Ramphastos toco yellow. Scale bars represent 5 µm (A,D–F) or 2 µm (B,C). Abbreviations: c, collagen macrofibrils; e, epidermis; l, lipid vacuoles; m, melanosomes.

View larger version (168K): [in a new window]   Fig. 7. Transmission electron micrographs of nanostructured arrays of dermal collagen from: (A) Oxyura jamaicensis, light blue; (B) Numida meleagris, dark blue; (C) Tragopan satyra, dark blue; (D) Tragopan caboti, dark blue; (E) Tragopan caboti, light blue; (F) Tragopan caboti, orange; (G) Syrigma sibilatrix, blue; (H) Ramphastos toco, dark blue; (I) Philepitta castanea, light blue; (J) Gymnopithys leucapsis, light blue; (K) Procnias nudicollis, green and (L) Terpsiphone mutata, dark blue. All images were taken at 30000x. All scale bars represent 200 nm.

View larger version (116K): [in a new window]   Fig. 8. Two-dimensional Fourier power spectra of transmission electron micrographs of nanostructured collagen arrays from: (A) Dromaius novaehollandiae, blue; (B) Tragopan satyra, dark blue; (C) Pilherodius pileatus, light blue; (D) Coua reynaudii, dark blue; (E) Ramphastos toco, dark blue; (F) Philepitta castanea, light blue; (G) Gymnopithys leucapsis, light blue; (H) Procnias nudicollis, green and (I) Dyaphorophyia concreta, yellow green. Colours (from blue to red) indicate the magnitude of the squared Fourier components, which are in dimensionless units. Ring diameter is inversely proportional to the peak wavelength of the coherently scattered colour.

View larger version (28K): [in a new window]   Fig. 9. Radial means of the two-dimensional Fourier power spectra of transmission electron micrographs of avian dermal collagen arrays: (A) Oxyura jamaicensis, light blue; (B) Tragopan temminckii, dark blue; (C) Tragopan temminckii, light blue; (D) Tragopan caboti, orange; (E) Coua reynaudii, dark blue; (F) Ramphastos toco, dark blue; (G) G. leucapsis, light blue; (H) Dyaphorophyia concreta, green and (I) Terpsiphone mutata, dark blue. The shaded zones show the range of spatial frequencies that are likely to produce coherent scattering of visible light wavelengths. G. leucapsis has a larger peak spatial frequency that falls outside the range of values likely to produce a visible colour by coherent scattering.

View larger version (48K): [in a new window]   Fig. 10. Comparisons of measured reflectance spectra (blue) and Fourier-predicted reflectance spectra (orange) for a sample of structurally coloured avian specimens: (A) Lophophorus impejanus, dark blue; (B) Tragopan temminckii, dark blue; (C) Tragopan temminckii, light blue; (D) Tragopan caboti, orange; (E) Syrigma sibilatrix, light blue; (F) Coua caerulea, dark blue; (G) Ramphastos toco, dark blue; (H) Selenidera culik, green and (I) Dyaphorophyia concreta, yellow-green. Reflectance spectra are reported as % reflectance (blue, left axis), and predicted reflectance spectra are reported as % visible Fourier power (orange, right axis).