Structural color change following hydration and dehydration of iridescent mourning dove (Zenaida macroura) feathers
Introduction
One important function of the metazoan integument is the display of color for crypsis or communication. While in many cases this color is static, changing only with age or environmental damage, in others it changes dynamically in response to background coloration (e.g., the skin of cephalopods; Hanlon, 2007), breeding condition (e.g., the skin of the toad Bufo luetkenii; Doucet and Mennill, 2009), excitation state (e.g., wattles of wild turkeys Meleagris gallopavo; Eaton, 1992), or in response to abiotic factors (e.g., to humidity in the beetle Tmesisternus isabellae; Liu et al., 2009).
The colors of feathers, while extremely diverse and frequently vivid, are thought to be largely static (Andersson and Prager, 2006). Feathers are composed of dead keratin tissue with no innervation or vascularization, and therefore cannot be under direct control of the animal or linked to other physiological processes. However, many of them contain highly organized tissues, or biophotonic nanostructures, that produce color not through pigments but through coherent light scattering (Prum, 2006). Because the refractive index, nanoscale size and arrangement of these nanostructures determine the colors they produce, they may be subject to change by external factors. For example, the replacement of air (refractive index (RI) = 1.00) by water molecules (RI = 1.33) in the biophotonic nanostructures of Morpho butterfly scales under high vapor pressure changes their refractive index contrast and hence color (Potyrailo et al., 2007). A few studies have shown that structural plumage colors can substantially change over longer periods of time from days to weeks (Montgomerie et al., 2001, Örnborg et al., 2002, Barreira et al., 2007, Shawkey et al., 2007, Delhey et al., 2010), and while in some cases “cosmetics” like colored preen oil may effect rapid changes (reviewed in Montgomerie, 2006), whether nanostructures can rapidly respond to simple environmental variables is largely unknown (but see Eliason and Shawkey, 2010).
Non-iridescent structural feather colors are typically created by matrices of keratin and air forming a single medullary layer (termed a “spongy layer“) within feather barbs, while iridescent colors are typically created by stacks of melanin granules within a keratin substrate in feather barbules (Prum, 2006). One of the simplest such structures is a single layer of melanin granules or air surrounded by an even keratin cortex that can produce a broad range of colors by thin-film interference (Prum, 2006). The color of these structures is largely determined by the thickness of the keratin cortex (Brink and van der Berg, 2004, Doucet et al., 2006, Shawkey et al., 2006, Yin et al., 2006, Nakamura et al., 2007). Since by definition iridescent colors change with the angle of incidence, the angle of barbules relative to incident light also affects color (Yoshioka and Kinoshita, 2002, Nakamura et al., 2007, Yoshioka et al., 2007). Because avian keratin is sensitive to hydration (Bonser, 2002), we hypothesized that wetting and drying of feathers may shrink or swell the keratin matrix of the barbules, changing their color through (i) alteration of the thickness of the outer keratin layer and/or (ii) twisting of barbules.
To test these hypotheses, we used iridescent neck feathers from mourning doves (Zenaida macroura Linnaeus 1758). These feathers appear pink/violet to the human eye and contrast with the brown feathers comprising the majority of the species’ plumage (Otis et al., 2008). We experimentally tested the response of reflected color (as measured by a UV–vis spectrometer) of these feathers to repeated rounds of wetting and drying. To understand the mechanistic basis of any changes, we used scanning and transmission electron microscopy (SEM and TEM) and thin-film optical modeling to first determine the morphological and physical basis of color production and then identify changes in this morphology after treatment.
Section snippets
Materials and methods
We pulled adjacent violet (iridescent) and brown (non-iridescent) captive-grown neck feathers from 24 different birds in an indoor captive population of mourning doves at the University of Utah. Because they were housed in indoor cages for the entire period of growth and afterwards, these feathers had only been exposed to small amounts of water. All feathers were stored in a climate-controlled room in opaque paper bags until analysis.
Results
At normal incidence, reflectance spectra of iridescent feathers were characterized by decreasing reflectance at short wavelengths and by a single peak whose wavelength (∼420 nm, see Table 1) we classify as hue and a short plateau at longer wavelengths (Fig. 1). In experiments STACK1 and STACK2, the color of iridescent feathers significantly changed following experimental rounds of wetting and drying (Table 1, Fig. 1A, D–F). In experiment STACK1, hue significantly decreased (Table 1, Fig. 1A and
Discussion
In this study we show that iridescent plumage color changes in response to water. Wetting and drying iridescent feathers noticeably and significantly increased their overall reflectance and chroma and changed their hue. The effects on achromatic color were stronger and more repeatable than those on chromatic color (hue).
The color-producing nanostructure of these feathers consists of a single thick layer of keratin cortex over a layer of air and melanosomes in barbules. The close match of
Acknowledgements
We thank R. Maia, M. Meadows and T. Hunt for useful discussions, D. Ott and B. Wang for assistance with microscopy, and two anonymous reviewers for helpful comments and suggestions. This work was supported by University of Akron startup funds and AFOSR grant FA9550-09-1-0159 (both to M.D.S.).
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