What makes a feather shine? A nanostructural basis for glossy black colours in feathers

Abstract

Colours in feathers are produced by pigments or by nanostructurally organized tissues that interact with light. One of the simplest nanostructures is a single layer of keratin overlying a linearly organized layer of melanosomes that create iridescent colours of feather barbules through thin-film interference. Recently, it has been hypothesized that glossy (i.e. high specular reflectance) black feathers may be evolutionarily intermediate between matte black and iridescent feathers, and thus have a smooth keratin layer that produces gloss, but not the layered organization of melanosomes needed for iridescence. However, the morphological bases of glossiness remain unknown. Here, we use a theoretical approach to generate predictions about morphological differences between matte and glossy feathers that we then empirically test. Thin-film models predicted that glossy spectra would result from a keratin layer 110-180 nm thick and a melanin layer greater than 115 nm thick. Transmission electron microscopy data show that nanostructure of glossy barbules falls well within that range, but that of matte barbules does not. Further, glossy barbules had a thinner and more regular keratin cortex, as well as a more continuous underlying melanin layer, than matte barbules. Thus, their quasi-ordered nanostructures are morphologically intermediate between matte black and iridescent feathers, and perceived gloss may be a form of weakly chromatic iridescence.

Figure 1.

(a) Diffuse (solid lines) and (b) specular (dashed lines) smoothed reflectance spectra of species with (a) glossy and (b) matte black plumage. (a) Black, double-crested cormorant; red, common raven; green, fish crow; blue, magpie-lark; light blue, acorn woodpecker; purple, Caspian tern; yellow, turkey vulture; grey, yellow-bellied sapsucker. (b) Black, yellow-billed cacique; red, horned grebe; green, Baltimore oriole; blue, northern flicker; light blue, black-mandibled toucan; purple, California quail; yellow, house sparrow; grey, American goldfinch. (c) Boxplot of glossiness values for glossy and matte species.

Figure 2.

Contour plot of the average reflectance and contrast of thin-film model simulations varying in both keratin cortex and melanin layer thicknesses. Measured values for glossy (circles) and matte (triangles) species are displayed, and ovals represent the standard deviation in both keratin cortex and melanin layer thicknesses (solid line, glossy; dashed line, matte).

Figure 3.

Comparison of (a,d) matte (California quail), (b,e) glossy (common raven) and (c,f) iridescent (boat-tailed grackle Quiscalus major, not included in this study) for (a–c) plumage properties and (d–f) barbule morphology, as observed through TEM (scale bars, 2 µm). Note the increasing order and continuity of the outermost melanin granules from right to left. Photo credits: (a) Matthew Knoth; (b) Jean-Guy Dallaire; and (c) Tom Friedel.

Figure 4.

Standardized effect sizes for (a) type of colour (glossy or matte) and (b) association with glossiness on the tested variables. In (a), effect sizes are relative to glossy species (i.e. positive values indicate higher values for glossy than matte species). Asterisks indicate (a) significant t-tests or (b) Pearson correlation tests (and 95% confidence intervals for effect size that do not overlap zero).

Figure 5.

(a) Boxplot for the roughness measurements obtained from visual evaluation of SEM images of glossy and matte feather barbules. (b–e) Examples of SEM images from glossy ((b) yellow-bellied sapsucker; (c) common raven) and matte ((d) horned grebe; (e) American goldfinch) barbules. Scale bars, 5 µm.