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INTRODUCTION
Over evolutionary time, metazoans, and birds in particular, have
occupied large portions of available color gamut, in part because
of the diversity of color production mechanisms available to them
(Stoddard and Prum, 2011). Coloration can result from selective
light absorption by pigments deposited in feathers. Although more
than five classes of pigments have been found in bird feathers, those
most commonly present are melanins and carotenoids (McGraw,
2006). Melanins, found within membrane-bound organelles
(melanosomes), can produce colors ranging from black to reddish
browns and pale oranges (McGraw, 2006). Carotenoid pigments
are acquired by birds through their diet (Goodwin, 1984) and are
responsible for most of the bright red, orange and yellow colors
(Brush, 1978). A second mechanism of color production is caused
by the interaction between incident light and nano-scale reflective
tissues (structural coloration) of feather barbs and barbules. Colors
produced in this manner include the blue, violet, ultraviolet (UV)
and iridescent parts of plumage (Auber, 1957; Dyck, 1976).
It has long been recognized that structural and pigment-based
colors are not mutually exclusive and can interact with one another
to attain colors not possible by either mechanism alone (Dyck,
1971a; Prum et al., 1999a). For example, the combination of
structural blue colors with yellow colors caused by pigments is
thought to give rise to most green plumage colors (Auber, 1957;
Fox, 1976) (but see Prum et al., 1998). Surprisingly, however,
with the exception of a few studies (Dyck, 1971a; Shawkey and
Hill, 2005; Shawkey and Hill, 2006), the interaction between
pigment and structure has not been examined in detail.
Understanding these interactions is crucial because different
mechanisms of plumage coloration vary in, for example, their
developmental cost and thus may convey different information
to conspecifics. Furthermore, they may provide inspiration for
new materials with novel optical properties.
As a result of over 150 years of captive breeding, the color
diversity of budgerigars [Aves, Psittacidae, Melopsittacus
undulatus (Shaw 1805); Fig.1A] now far exceeds that of their
green wild ancestors (Taylor and Warner, 1986). Color morphs
include achromatic whites and greys as well as chromatic colors
ranging from purple to yellow (World Budgerigar Organisation,
www.world-budgerigar.org/). These latter colors are thought to
be produced through various combinations of both nanostructures
and pigment (Simon, 1971; Parker, 2002), but as far as we are
aware, no data exist to support this hypothesis. Because of their
diversity in color and (potentially) color production mechanisms,
as well as rich genetic data from breeders, budgerigars may serve
as a model system for understanding both physical and genetic
bases of color evolution. Here, we use multiple techniques to
identify the physical bases of color production in seven morphs
of the budgerigar to determine the relative contribution of
pigments and structure to plumage color.
The Journal of Experimental Biology 215, 1272-1277
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.064907
RESEARCH ARTICLE
Relative contributions of pigments and biophotonic nanostructures to natural color
production: a case study in budgerigar (Melopsittacus undulatus) feathers
Liliana DʼAlba*, Leah Kieffer and Matthew D. Shawkey
Department of Biology and Integrated Bioscience Program, University of Akron, Akron, OH 44325-3908, USA
*Author for correspondence (liliana@uakron.edu)
Accepted 13 December 2011
SUMMARY
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 ʻspongy
layerʼ 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.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/215/8/1272/DC1
Key words: structural color, psittacofulvin.
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