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First published online January 3, 2006
Journal of Experimental Biology 209, 380-390 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.01988
Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour
1 Department of Biological Sciences, 331Funchess Hall, Auburn University,
Auburn, AL 36849, USA
2 Department of Biology, Queen's University, Kingston, ON, Canada K7L
3N6
* Author for correspondence (e-mail: doucets{at}auburn.edu)
Accepted 15 November 2005
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Summary |
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Key words: feather, barbule, structural colour, iridescence, thin-film modeling, bird
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
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). Both mechanisms
of colour production are widespread in birds. Colours produced by feather
nanostructures, termed structural colours, can be further subdivided into
iridescent and non-iridescent colours. Broadly defined, iridescent structural
colours change in appearance with angle of observation or illumination, while
non-iridescent colours generally remain similar in appearance regardless of
viewing geometry (Newton,
1730; Osorio and Ham,
2002). Both types of structural plumage colour can be produced by
coherent scattering of light waves within feathers, but these two types of
colouration differ in the composition and organization of their
light-scattering elements (Prum,
2006).
Non-iridescent structural colours are generally produced in feather barbs.
Two-dimensional Fourier analysis has revealed that quasi-ordered arrays of
keratin and air within feather barbs are likely responsible for producing the
turquoise, blue, violet, and ultraviolet colours found in a number of species
(Prum et al., 1998,
1999,
2003;
Shawkey et al., 2003;
Doucet et al., 2004). By
contrast, iridescent structural colours are generally produced in feather
barbules (Prum, 2006), where
light is scattered constructively by laminar or crystal-like arrays consisting
of alternating layers of materials with different refractive indices, namely
keratin, melanin and air.
Although all iridescent plumage colours are produced by the same underlying
mechanism, considerable variation exists in the structure and arrangement of
the alternating layers of keratin and melanin and, consequently, in the
appearance of different iridescent colours. The melanin granules can be rodor
disk-shaped, solid or hollow, and arranged in single or multiple layers
(Durrer, 1986;
Prum, 2006). The brilliantly
coloured iridescent gorgets of many hummingbird species, for example, are
produced by the coherent scattering of light from multiple, alternating layers
of keratin and air-filled, disk-shaped melanin granules
(Greenwalt et al., 1960;
Land, 1972). The
multi-coloured iridescent eye spots on the tails of male green peacocks
Pavo muticus, by contrast, are produced by crystal-like arrays of
rod-shaped melanin granules (Zi et al.,
2003).
In some species, iridescence is achieved by a single pair of keratin and
melanin layers. Using thin-film optical modeling based on nanostructural
barbule measurements, Brink and van der Berg
(2004) recently showed that the
coppery-purple iridescence of the plumage of hadeda ibises Bostrychia
hagedash is produced primarily by coherent scattering from an unusually
thick (
0.8 µm) and uniform keratin cortex. The single, underlying
layer of elliptical melanin platelets apparently serves mainly to define the
thickness of the superficial keratin layer
(Brink and van der Berg, 2004).
A number of species with iridescent plumage share similarities in barbule
microstructure with the hadeda ibis; that is, they contain a single
superficial layer of keratin overlying either a single layer, or a solid
cluster, of melanosomes (Durrer,
1986; Prum, 2006).
Whether these other species produce iridescence by the same mechanistic
process, however, remains to be investigated.
Here, we investigate the mechanisms of colour production in the iridescent
plumage of satin bowerbirds Ptilonorhynchus violaceus minor Campbell
1912. Adult male satin bowerbirds have glossy, iridescent plumage that appears
violet-blue to the human eye and reflects maximally at ultraviolet wavelengths
(Doucet and Montgomerie,
2003b). Males exhibit delayed plumage maturation whereby juvenile
males molt into a female-like green plumage each year until their seventh
calendar year, when they molt into the iridescent plumage characteristic of
adult males (Vellenga, 1980).
Male plumage colouration may be a sexually selected indicator of quality in
this species, as plumage is sexually dichromatic and variation in plumage
colouration relates positively to the expression of other sexual ornaments as
well as various indicators of health and condition (Doucet and Montgomerie,
2003b,c).
While some studies suggest that iridescent and non-iridescent structural
colouration may be condition-dependent in some species
(Keyser and Hill, 1999; e.g.
Doucet, 2002;
McGraw et al., 2002;
Hill et al., 2005), the
microstructural mechanisms responsible for condition-dependent variation in
structural colour remain a matter of debate
(Fitzpatrick, 1998;
Andersson, 1999; Prum,
1999,
2006). Shawkey et al.
(2003) recently showed that in
male eastern bluebirds Sialia sialis, intraspecific variation in
non-iridescent structural plumage colouration is associated with the density
and uniformity in size of nanostructural elements within the colour-producing
keratin matrix of feather barbs. These findings suggest that stress-induced
disruption of barb nanostructure during feather growth could be manifested in
plumage colouration, thereby highlighting a mechanism whereby non-iridescent
structural colours could reveal quality
(Fitzpatrick, 1998;
Andersson, 1999;
Shawkey et al., 2003).
However, the self-assembly mechanisms guiding the organization of
colour-producing nanostructures in developing feathers may limit their
sensitivity to environmental perturbation
(Prum, 2006).
We had three objectives in this study of iridescent plumage colouration in satin bowerbirds. First, we used scanning- and transmission-electron microscopy to characterize the barbule microstructure of adult males, using barbules of juvenile males as a basis for comparison. Second, based on measurements from microscopic imaging, we used thin-film optical models to identify the mechanisms responsible for creating the iridescent ultraviolet colouration of adult males. Finally, we used spectrometry and nanostructural barbule measurements to investigate the relationship between individual variation in barbule nanostructure and iridescent plumage colour in satin bowerbirds.
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). We captured birds near active bowers using
mist nets baited with blue objects. We marked individuals with a unique
combination of three coloured leg bands and a stainless steel band (Australian
Bird and Bat Banding Scheme). We removed 6–10 rump feathers from each
individual, placed them in paper envelopes, and stored them in a cool, dry
place for later analysis. We performed detailed spectrometric and microscopic
analysis of feathers from 10 adult males. As a basis for comparison, we also
include digital photographs and scanning- and transmission-electron images of
non-iridescent green feathers of a single juvenile male from the same
population.
Spectrometry
We taped feathers onto matte black cardboard for spectrometric analysis,
arranging the feathers in an overlapping fashion to approximate their usual
configuration on a bird's body. We measured the reflectance of these feathers
using an S2000 spectrometer and deuterium tungsten-halogen light source (Ocean
Optics, Dunedin, FL, USA). All measurements were taken with unpolarized light.
We took readings using a bifurcated fibre-optic cable mounted in a
metal-encased probe that transmitted incident light to the measurement area
and reflected light to the spectrometer. The probe was mounted in a rubber
sheath that excluded ambient light and maintained the probe at a fixed angle
perpendicular to the feather surface, where both incident
(
i) and reflected (r) light angles=0°
(see Fig. 1). This measurement
geometry was used for all measurements except those specifically intended to
determine the effects of varying the angle of incidence (see below). Using
OOIBase32 software (Ocean Optics), we took five readings from each feather
sample, with each reading comprising an average of 20 spectra measured
sequentially. All measurements were expressed as percent reflectance relative
to a Spectralon white standard (WS-1; Ocean Optics). We summarized our
reflectance data by calculating four tristimulus colour variables to
approximate three dimensions of colour: hue, brightness and spectral purity
(Hailman, 1977;
Montgomerie, 2006). We
calculated hue as the wavelength of maximum reflectance in the bird-visible
spectrum, from 300 to 700 nm (Cuthill et
al., 2000; Hart,
2001). We calculated brightness as the maximum percent reflectance
from 300 to 700 nm (percent reflectance at peak wavelength). We calculated two
measures of spectral purity. The first, which we term `saturation', was
calculated as the quotient of the maximum reflectance minus the minimum
reflectance divided by the total reflectance. This value should provide a
measure of saturation that is independent of hue. The second measure of
spectral purity, which we term `UV-chroma', was calculated as the proportion
of reflectance in the UV portion of the spectrum (from 300 to 400 nm). We
calculated UV-chroma as it has been used previously to investigate the signal
function of variation in colour in satin bowerbirds (Doucet and Montgomerie,
2003b,c).
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To investigate the influence of measurement geometry on variation in reflectance, and the capacity of thin-film modeling to account for this variation, we remeasured the feathers of a single individual using separate fibre optic cables for transmitting incident and reflected light (see Fig. 1). Using an angled fibre holder (AFH-15, Avantes Inc., Boulder, CO, USA), we measured the reflectance of feathers at matching incident and reflected light angles of 15°, 30°, 45°, 60° and 75°.
Digital photography
We took digital photographs of feathers using a QImaging Micropublisher RTV
3.3 firewire camera (Burnaby, BC, Canada) connected to an Olympus SZ11
dissecting microscope (Melville, NY, USA). We collected images through an
ImageJ TWAIN plugin provided by Qimaging.
Scanning electron microscopy
We mounted feathers on stubs with carbon tape (Ted Pella, Redding, CA,
USA), sputter-coated them with gold on an Electron Microscopy Sciences sputter
coater (Hatfield, PA, USA), and viewed them on a Zeiss DSM 930 Scanning
Electron Microscope (Oberkochen, Germany).
Transmission electron microscopy
We prepared barbules from the rump feathers of 10 adult males for
transmission electron microscopy (TEM) following Shawkey et al.
(2003). We also embedded and
sectioned the barbules of one juvenile male to allow for visual comparisons of
differences in barbule ultrastructure between adults and juveniles. Using a
Philips EM301 transmission electron microscope (Veeco FEI Inc, Hillsboro, OR,
USA), we took micrographs of cross-sections of feather barbules at 2500x
magnification. To calibrate the images, we took micrographs of a
waffle-pattern diffraction grating (Ted Pella, Redding, CA, USA), accurate to
1 nm ±5% at the same magnification. We scanned these micrographs at 400
d.p.i. using an Epson Perfection 1240U flatbed scanner and used NIH Image v
1.62 (available for download at
http://rsb.info.nih.gov/nih-image/index.html)
to measure six nanostructural variables
(Fig. 3E,
Table 1). (1) We measured the
thickness of the keratin cortex and (2) the thickness of the outer melanin
layer at six evenly spaced points surrounding each barbule. We defined the
outer melanin layer as the layer including all melanin granules that,
beginning at the cortex, were contiguous with other melanin granules. (3) We
also counted the number of melanin granules encountered at each of the six
measurement locations of the thickness of the outer melanin layer, so that we
could calculate the mean number of melanin granules comprising the melanin
layer. (4) We measured the thickness of each barbule at three evenly spaced
locations along the width of the barbule. (5) To estimate the percentage of
melanin in the outer layer, we used Carnoy (available at
http://www.kuleuven.ac.be/bio/sys/carnoy/)
to measure the cross-sectional area of melanin in the outer layer. We divided
this value by the total cross-sectional area of the outer layer to obtain a
measure of the percentage of melanin in the outer layer. (6) Using a similar
approach, we obtained a measure of the percentage of melanin in the center of
barbules, beneath the outer layer. For simplicity, we refer to this latter
measurement as the percentage of melanin in the inner layer
(Table 1). We measured five
barbules for each adult male and used mean values in our analyses.
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Thin-film optical modeling
We used a standard transfer matrix thin-film optical model
(Jellison, 1993) to determine
how iridescent colour is produced in satin bowerbirds (see model details in
Appendix). We used this model to predict the reflectance spectra of feathers
from the thickness and optical properties of keratin and melanin layers,
allowing us to evaluate the relative importance of these layers in determining
reflectance characteristics and providing insight into how variation in each
might affect colouration. We used previously published, empirically estimated
refractive indices of air (n=1.00), keratin (n=1.56) and
eumelanin (n=2.00) (Land,
1972; Brink and van der Berg,
2004), estimated lower limit extinction coefficients for keratin
(k=0.03) and eumelanin (k=0.6)
(Brink and van der Berg, 2004),
as well as angles of incidence and reflectance matching those of our measured
spectra in all of our calculations. Although we used unpolarized light for our
spectral measurement, the Appendix includes formulae for both s- and
p-polarized light. At smaller angles of incidence, models calculated from s-
and p-polarized light predicted very similar reflectance spectra. However,
Brewster angles ranging between 38° and 57° (calculated as
tan-1(n2/n1), where
n2 and n1 are the refractive indices
of the respective media) predict that the p-component will largely disappear
at initial angles of incidence greater than 40°. Because of this effect,
and because reflectance spectra predicted by s- and p-polarization were
similar up to initial angles of incidence of 40°, we present only model
results from s-polarization.
We created four hypothetical thin-film reflectance models, using all possible two- and three-beam combinations for the upper surface of the barbule (Fig. 2). Model 1 included all three interfaces of materials of different refractive indices (air/keratin, keratin/melanin, melanin/keratin) and the thicknesses of the keratin and melanin layers. Model 2 included only the outer two interfaces (air/keratin, keratin/melanin) and the thickness of the keratin layer. Model 3 included only the air/keratin and melanin/keratin interfaces, and the thickness of the melanin layer. Model 4 included only the inner two interfaces (keratin/melanin, melanin keratin) and the thickness of the melanin layer. We visually compared the spectra produced by these models to measured reflectance spectra from the feathers. For the model with the best predictive ability, we compared hues generated by the model to measured hues across individual males.
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Statistical analyses
Descriptive statistics are reported as means ± standard error
(s.e.m.). To determine whether variation in barbule microstructure could
predict variation in colour, we constructed stepwise regression models using a
backward elimination procedure. We constructed three models, each with a
different colour variable (hue, UV-chroma and brightness) as the independent
variable. In each model, we used cortex thickness, the thickness of the outer
melanin layer, the percentage of melanin in the outer layer, the percentage of
melanin in the inner layer, and barbule thickness as potential predictor
variables. Probabilities to leave the model were set at 0.05.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
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Thin-film optical modeling
Model 2 generated predicted reflectance spectra that closely matched
measured spectra from bowerbird feathers
(Fig. 4). This model
incorporated only the thickness of the keratin cortex and its associated
interfaces (air/keratin and keratin/melanin). Spectra predicted from Model 2,
despite exhibiting slightly narrower and lower reflectance peaks, were
strikingly similar to measured spectra
(Fig. 4). The other three
models, which included all other possible combinations of the three layers
(air, keratin and melanin) and their associated interfaces, generated
predicted reflectance spectra that poorly matched measured spectra
(Fig. 4). Considerable changes
in the values of the extinction coefficients and refractive indices of the
different layers did not substantially improve the fit of these models to
predicted spectra (M. D. Shawkey, unpublished data). Moreover, modifying the
extinction coefficients of keratin and melanin
(Fig. 5A) or the refractive
index of melanin (Fig. 5B) did
not substantially change the predictive ability of Model 2. These results
strongly suggest that scattering of light by the outer cortex layer alone is
sufficient to cause the observed colour of adult male satin bowerbird
feathers, regardless of minor fluctuations in the optical properties of the
scattering elements. If we expand our thin-film model matrices to include
infrared wavelengths, Model 2 predicts a fundamental peak at 1325 nm
(Fig. 6), well beyond the
bird-visible range. Thus, the peak of reflectance within bird-visible
wavelengths is actually a second order harmonic of the fundamental peak.
Models 1, 3, and 4 predict fundamental peaks at 855 nm, <300 nm and1311 nm,
respectively.
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In Model 2, the only parameter likely to vary between individuals was cortex thickness, as the only other variables incorporated in the model–the refractive indices and extinction coefficients of the different layers–are expected to remain constant across individuals. Changing cortex thickness in the model resulted in reflectance spectra with identical shapes that were shifted to longer or shorter wavelengths when cortex thickness was increased or decreased, respectively. We calculated predicted hues (wavelength at maximum reflectance) from reflectance spectra generated by Model 2 based on each individual's mean measured cortex thickness (Table 2) and compared these to measured hues for those individuals (Fig. 7). Both predicted and measured hues varied linearly with cortex thickness (Fig. 7), and there was a significant positive correlation between predicted and measured hues (r=0.64, N=10, P=0.04).
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Microstructure and individual variation in colour
Cortex thickness significantly predicted hue, such that males with thicker
barbule cortexes had plumage reflectance that peaked at longer wavelengths
(Table 3). The percentage of
melanin in both the outer and inner layers significantly predicted UV-chroma,
such that individuals with greater densities of melanin in their barbules had
plumage that reflected proportionally more in the UV
(Table 3). None of the
nanostructural variables significantly predicted plumage brightness
(Table 3; all
P>0.26).
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Discussion |
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Compared with the non-iridescent barbules of juvenile males, the iridescent
barbules of adult male satin bowerbirds are enlarged, elongated, flattened and
twisted at the base so that the flattened surface of the barbules is parallel
with the surface of the feathers. Moreover, the barbules of adult males have a
thin cortex of uniform thickness whereas those of juveniles have a thick,
irregular cortex. These differences in barbule microstructure highlight the
remarkable change in appearance that accompanies sexual maturation in this
species. Olive-green plumage can be caused by the deposition of carotenoid
pigments in the barbs and melanin pigments in the barbules, or by the
combination of a blue-producing keratin matrix and yellow carotenoid pigments
in the barb (Dyck, 1978).
Because the barbs of juvenile male satin bowerbirds have a greenish
appearance, the latter mechanism is likely responsible
(Dyck, 1978), though this
hypothesis requires further confirmation. Thus, when molting from their
juvenile to adult plumages, males switch to an entirely different colour
production mechanism, from a non-iridescent green colour produced in the barbs
to an iridescent ultraviolet colour produced in the barbules.
Specialized barbule morphology, as exemplified by the flattened, twisted
barbules of adult male satin bowerbirds, is widespread among birds with
iridescent colour and likely plays a role in enhancing the efficiency of
iridescent colour displays (Osorio and
Ham, 2002; Brink and van der
Berg, 2004; Prum,
2006). In satin bowerbirds, males build avenue-shaped bowers of
small twigs. Males perform courtship displays on a decorated platform directly
in front the bower avenue, and females observe displaying males from within
these avenue walls (Borgia,
1986). Thus, females necessarily observe displaying males from a
fixed viewing geometry. In our rainforest population, males build their bowers
where tree falls or human disturbance have created a canopy gap, orienting
their bowers such that they face away from these gaps and upslope
(Doucet and Montgomerie,
2003a). This configuration maximizes the frontal illumination of
males during courtship displays. According to our spectral measurements, this
viewing geometry, which corresponds to small angles of incident and reflected
light, would result in highly saturated and relatively bright male plumage
reflectance for body regions facing the female. Females would also observe
occasional bright flashes of reflectance (specular highlights or glare) as the
males perform their ritualized courtship displays. Most importantly, this
viewing geometry ensures that male plumage will always show some
interference-based reflectance. By contrast, increasing the angle of incidence
without simultaneously increasing the angle of reflected light (as would occur
if male bowerbirds were illuminated from above or behind) results in
increasingly dull and unsaturated reflectance spectra that are
indistinguishable from black at angles of incidence >45° (S. M. Doucet,
unpublished data). Similarly, the association of the bower location with a
canopy gap likely enhances the plumage display, as males often appear black
rather than blue under the cover of dense rainforest canopy (S. M. Doucet,
personal observation). Among other species with iridescent colouration,
barbules are tilted away from the exposed surface of the feather such that
different combinations of illumination and viewing angles result in the
brightest or most saturated reflectance
(Osorio and Ham, 2002). The
crown feathers of the magnificent hummingbird Eugenes fulgens, for
example, have barbules that are tilted at 42° away from the surface of the
feather, resulting in the brightest and most saturated reflectance when
illuminated from above and viewed from directly in front of a displaying bird
(Osorio and Ham, 2002). A
comparative investigation of barbule structure and display orientation among
iridescent species would provide fascinating insights into the strength of
selection for behavioural and morphological modifications that enhance
iridescent colour displays.
Thin-film Model 2, which incorporated only properties of the keratin cortex
and its associated interfaces, predicted reflectance spectra that closely
matched measured spectra. The other three models predicted reflectance spectra
that were much flatter, slightly brighter and, in all but one case, of a very
different shape, than measured spectra. Although the refractive indices of
keratin and air are well established
(Land, 1972), the refractive
index of eumelanin has only recently been empirically determined
(Brink and van der Berg, 2004),
and the extinction coefficients of keratin and melanin are lower-limit
estimates based on a single study (Brink
and van der Berg, 2004). Our data show, however, that the
predictive abilities of the other models cannot be substantially improved by
changing these variables, and that the predictions of Model 2 are relatively
robust to such changes. The melanin layer of satin bowerbird barbules is so
thick and densely packed that it likely absorbs most of the light that reaches
it and thus plays a limited role in creating iridescence, serving primarily to
delineate the thickness of the cortex. This likely explains why the other
three models, all of which included scattering from the melanin layer, could
not accurately predict bowerbird reflectance spectra. Correspondingly, models
incorporating layers below the outer melanin layer also failed to predict
satin bowerbird reflectance spectra (M. D. Shawkey, unpublished data). Our
findings therefore suggest that, as in the hadeda ibis
(Brink and van der Berg, 2004),
the iridescent colour of adult male satin bowerbirds is produced primarily by
constructive interference of light within the barbule cortex. The interference
of light predicted by the other models, particularly Model 1, may subtly
influence the shape of reflectance spectra, but they are unlikely to
contribute to variation in hue.
Measured reflectance spectra were slightly brighter and less saturated than those predicted by the best model (Model 2). However, this model assumed idealized reflectance from a single barbule, whereas we measured reflectance from several barbules at once. One possible explanation is that the slight discrepancy between the curves may have been caused by subtle variation in the orientation of the reflecting surface of barbules on the feathers that we measured. Because changes in measurement geometry lead to concurrent changes in hue, brightness and saturation, subtle variation in the orientation of barbules might explain the broader and brighter peaks of measured spectra. Our model also makes the assumption that the melanin layer is uniform. However, keratin fills the small spaces between melanin granules. This heterogeneity of the melanin layer may result in the dephasing of light waves entering this layer, producing incoherent scattering that would decrease saturation and broaden reflectance peaks. This interpretation receives indirect support from the observation that individuals with more densely packed melanin granules exhibit plumage reflectance with greater UV chroma (see below).
Model 2 predicted hue closely, often within 10 nm ofmeasured hue. Indeed,
there was a significant positive correlation between hues predicted from the
model, based on each individual's cortex thickness, and hues calculated from
reflectance spectra. Two individuals deviated noticeably from the hues
predicted by their cortex thickness. Such a discrepancy could occur if the
barbules we sectioned were not representative of typical barbules in that
individual, if the barbule cross-sections were not exactly perpendicular, or
if the barbules were sectioned near the proximal end, which exhibits reduced
iridescence. Increasing the angle of incidence (and reflectance) of our
measurements resulted in a significant, linear decrease in hue. Model 2
predicted a similar decrease in hue with increasing angle of incidence, as
shown by the positive association between measured and predicted hues at 6
different angles of incidence. Such a shift toward shorter-wavelength hues is
expected from thin-film optical theory, as changing the angle of incidence
effectively changes the thickness of the thin-film layers
(Land, 1972). Not
surprisingly, similar shifts to shorter wavelengths with increasing angles of
incidence have been reported in a number of species with iridescent plumage
colouration (Cuthill et al.,
1999; Osorio and Ham,
2002; Brink and van der Berg,
2004).
Model 2 predicts a fundamental peak of reflectance at near-infrared
wavelengths, suggesting that the peak of reflectance that we measured is a
second-order harmonic of this near-infrared peak. It should be noted, however,
that the fundamental peak in the infrared is unlikely to play any role in
signaling, as it is beyond wavelengths that can be detected by birds
(Cuthill et al., 2000;
Hart, 2001).
Although the structural colouration of satin bowerbirds and hadeda ibises
appears to be produced by the same functional, one-layer mechanism, the
resulting reflectance spectra, and hence appearance of these birds, is
remarkably different. We have shown that this difference is caused solely by
the difference in cortex thickness between the species. As is true of all
thin-film optical structures
(Vacísek, 1960),
adjustment of the thickness of a material with particular refractive and
absorptive properties creates strikingly different colours. The apparent
simplicity of this mechanism for variation suggests that iridescent colours,
once evolved, may diverge rapidly during speciation
(Prum, 2006). Indeed, a recent
study suggests that the interspecific diversity of iridescent colours among
closely related cowbird species in the genus Molothrus (from glossy
violet to green) evolved primarily through changes in cortex thickness,
following a shift from matte black to iridescent through the rearrangement and
loss of melanin granules (M. D. Shawkey, M. E. Hauber, L. K. Estep, and G. E.
Hill, manuscript submitted for publication). Thus, subtle modifications of
this simple, single-layer mechanism have enabled the evolution of myriad
colours.
Whether and how iridescent colours might be used as condition-dependent
sexual signals remain controversial
(Andersson, 1999;
Osorio and Ham, 2002;
Prum, 2006). An important
first step to addressing these questions involves identification of the
microstructural mechanisms responsible for causing intraspecific variation in
colour (Shawkey et al., 2003;
Shawkey and Hill, 2005;
Hill et al., 2005). As
expected from our thin-film optical models, variation in hue was significantly
predicted by cortex thickness. Additionally, UV-chroma was significantly
predicted by the percentage of melanin in both the outer and inner layers of
the barbule. When incident light penetrates beyond colour-producing
nanostructures (in this case, the keratin cortex), the tissues below these
nanostructures can scatter light incoherently, reducing the overall saturation
of the colour (Prum, 2006).
Presumably, an increase in the density of melanin reduces the amount of
incident light that can penetrate beyond the cortex, thereby reducing the
amount of incoherent scattering and increasing the UV-chroma of the colour. We
have thus identified two aspects of barbule microstructure that predict
intraspecific variation in iridescent colour. If these microstructural
variables are associated with genetic quality, are sensitive to physiological
stress during feather development, or both, they could represent a means by
which iridescent structural colours may honestly signal quality in satin
bowerbirds (Doucet and Montgomerie,
2003b) and other species. None of our measures of barbule
microstructure significantly predicted brightness. Identifying a relationship
between barbule microstructure and brightness may require the measurement of
reflectance from individual barbules. Alternatively, brightness might relate
to larger-scale factors (Shawkey et al.,
2003), such as the number of coloured barbules on feathers or the
condition of these barbules, which could in turn be influenced by barbule
loss, breakage or abrasion. Hence, iridescent colouration could also be
informative if there is individual variation in susceptibility to feather
damage (Osorio and Ham, 2002).
Clearly, more research is needed in this area. Convincing evidence of direct
condition-dependence of structural colouration would require an experimental
demonstration of the effects of stress during feather growth on both
microstructure and colour.
Our results have implications for investigations of iridescent plumage colouration at both proximate and ultimate levels. At a proximate level, our study complements and extends other recent work on the physical mechanisms of iridescent colour production and lays a methodological foundation for the elucidation of the mechanistic basis for iridescence in other taxa. At an ultimate level, our study provides tantalizing evidence that at least some of the tremendous diversity of iridescent colours in birds can evolve through relatively minor variation in feather nanostructure. Future studies should use large-scale phylogenetic analyses to explicitly examine the evolution of structural colour mechanisms. Furthermore, we have identified nanostructural mechanisms responsible for creating intraspecific variation in iridescent colour, providing further insight into how these colours might evolve as signals of individual quality.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
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),
we treated each interface as matrices of the form:
 | (1) |
 |
j and
j–1 are the complex angles of incidence, calculated
using Snell's law:
ñ0sin0=ñjsinj.
The transfer matrix incorporated the thickness of the jth layer:
 | (3) |
djñjcosj)/
,
where dj is the thickness of the layer, and is
the wavelength of light.
The total scattering matrix is then given by:
 | (4) |
 | (5) |
 | (6) |
|
Acknowledgments |
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|
Footnotes |
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Present address: Department of Environmental Science, Policy and
Management, 137 Mulford Hall, #3114, University of California, Berkeley, CA
94720-3100, USA 
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References |
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