Structural Color Production by Constructive Reflection From Ordered Collagen Arrays

Ordered hexagonal arrays of parallel collagen fibers produce the brilliant green structural color of the fleshy, supraorbital caruncles of male Velvet Asity (Philepitta castanea; Aves: Eurylaimidae). The collagen arrays are organized in larger macrofibrils that are packed irregularly within cone-shaped papillae that cover the surface of the caruncle. The color of the caruncle conforms closely to the wavelengths predicted by applying Bragg's Law of constructive reflection to measurements of the size and spatial organization of the collagen arrays. These observations constitute a novel mechanism of structural color production in animals. These collagen arrays are convergently similar to the smaller, highly structured collagen arrays in the mammalian cornea, which exploit the same physical mechanism to produce optical transparency. @ 1994 Wiley-Liss, Inc. Structural colors of animals are produced by the interaction of light with organic and inorganic materials of different optical densities. The known mechanisms of structural color production in animals include diffraction from colloids of liquids, solids, or gases, and constructive reflection from ordered layers or films of mucus, keratin, chitin, melanin granules, or intracellular purine crystals (Fox, '76). In birds, the only documented structural colors are produced by ordered layers of melanin granules or air vacuoles within the keratin of feathers (Durrer, '62, '77, '84; Durrer and Villiger, '66; Lucas and Stettenheim, '71; Dyck, '76, '87). However, structural color production in the dermis of birds has not been analyzed in detail. Structural blue colors in bird skin have been hypothesized to be produced by Tyndall scattering, but the anatomical basis of these colors has never been described (Rawles, '60: 223; Lucas and Stettenheim, '72:406, 410; Fox, '76; Durrer, '84). This investigation documents a novel mechanism of structural color production based on the optical properties of ordered collagen fibers. Collagen is one of the most abundant and structurally important proteins in animals, but it is not presently known to contribute to production of any wavelength-specific structural color. However, the optical properties of collagen do contribute to its functional role in many organisms. Whiteness can be produced by reflection of incident light on unordered collagen fibers which vary in diameter and spacing. Structures such as the sclera of the human eye and the dermis of white axolotls appear white by this mechanism (Fox, '76; Vaezy and Clark, '91). Conversely, transparency of the vertebrate cornea is achieved by destructive interference among reflections from small, uniformly sized parallel collagen fibers in quasi-ordered arrays (Maurice, '57; Hart and Farrell, '69; Cox et al., '70; Benedek, '71; Vaezy and Clark, '91). The novel structural color described here is found in the Velvet Asity (Philepitta castanea; Aves: Eurylaimidae; formerly Philepittidae): a frugivorous, suboscine perching bird in a small subfamily (Philepittinae) that is endemic to the island of Madagascar (Amadon, '79; Langrand, '91; Prum, '93). We first describe the color and anatomy of the caruncles of Philepitta castanea and then present a model for the production of the obRandall L. Morrison is now at the Department of Biology, Hood College, 401 Rosemont Avenue, Frederick, MD 21701. ( 1 1994 WILEY-LISS, INC.