Relative contributions of pigments and biophotonic nanostructures to natural color production: a case study in budgerigar (Melopsittacus undulatus) feathers.

Understanding the mechanistic bases of natural color diversity can provide insight into its evolution and inspiration for biomimetic optical structures. Metazoans can be colored by absorption of light from pigments or by scattering of light from biophotonic nanostructures, and these mechanisms have largely been treated as distinct. However, the interactions between them have rarely been examined. Captive breeding of budgerigars (Aves, Psittacidae, Melopsittacus undulatus) has produced a wide variety of color morphs spanning the majority of the spectrum visible to birds, including the ultraviolet, and thus they have been used as examples of hypothesized structure-pigment interactions. However, empirical data testing these interactions in this excellent model system are lacking. Here we used ultraviolet-visible spectrometry, light and electron microscopy, pigment extraction experiments and optical modeling to examine the physical bases of color production in seven budgerigar morphs, including grey and chromatic (purple to yellow) colors. Feathers from all morphs contained quasi-ordered air-keratin 'spongy layer' matrices, but these were highly reduced and irregular in grey and yellow feathers. Similarly, all feathers but yellow and grey had a layer of melanin-containing melanosomes basal to the spongy layer. The presence of melanosomes likely increases color saturation produced by spongy layers whereas their absence may allow increased expression of yellow colors. Finally, extraction of yellow pigments caused some degree of color change in all feathers except purple and grey, suggesting that their presence and contribution to color production is more widespread than previously thought. These data illustrate how interactions between structures and pigments can increase the range of colors attainable in birds and potentially in synthetic systems.