Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage
1 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY
14853, USA
2 Department of Biological Sciences, Binghamton University, Binghamton, NY
13902, USA
3 Department of Biological Sciences, Simon Fraser University, Burnaby, BC
V5A 1S6, Canada
4 Department of Integrative Biology, Museum of Vertebrate Zoology,
University of California, Berkeley, CA 94720, USA
* Author for correspondence (e-mail: kjm22{at}cornell.edu)
Accepted 23 August 2002
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Summary |
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Key words: brown-headed cowbird, house sparrow, Molothrus ater, Passer domesticus, condition-dependent, ornamental trait, plumage
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Introduction |
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Plumage coloration in most birds comes in three distinct forms:
carotenoid-based, melanin-based and structurally based colors
(Fox and Vevers, 1960). The
most thoroughly investigated of all three ornament types, from both the
proximate and ultimate perspectives, are carotenoid-based signals, which
include most of the red, orange and yellow colors seen in animals
(Brush, 1978
). Carotenoid
pigments must be obtained in the diet before being deposited in the integument
(Goodwin, 1984
). Because
carotenoids are thought to be scarce in nature
(Grether et al., 1999
),
variation in the expression of carotenoid ornaments typically reflects the
nutritional condition of male birds at the time of molt (e.g.
Hill and Montgomerie, 1994
;
Hill, 2000
). Females from many
species prefer to mate with males that exhibit the brightest carotenoid-based
displays (for a review, see Olson and
Owens, 1998
; Hill,
1999
).
Melanin-based color displays (e.g. blacks, browns) have recently begun to
receive equal empirical consideration. Historically, most studies have
emphasized the link between social aggression and the degree to which melanin
ornaments are exaggerated (e.g. Rohwer,
1975,
1977
). In a variety of avian
species, males displaying the largest melanin-based badges are behaviorally
dominant to those having smaller color patches (for a review, see
Senar, 1999
). More recent work
has focused on the physiological constraints that may be associated with
producing melanin pigments. Early research suggested that there might be
nutritional limitations to growing large patches of feathers pigmented with
melanin (Veiga and Puerta,
1996
). Since then, there has been little experimental support for
the idea that melanin pigments are nutritionally or energetically expensive to
produce (Gonzalez et al.,
1999
; McGraw and Hill,
2000
). Moreover, there is equivocal evidence that females use
variation in the expression of melanin ornaments in their mating decisions
(e.g. Møller, 1988
;
Veiga, 1993
;
Kimball, 1996
;
Cordero et al., 1999
;
Griffith et al., 1999
).
Clearly, more research is needed to better understand the costs associated
with the production of melanin-based ornamental traits.
The function of structurally based color ornaments in birds remained
virtually unstudied until the last few years. Structural colors include the
blue, violet, ultraviolet and iridescent patches of feathers and skin
(Auber, 1957;
Dyck, 1974
). In contrast to
the pigment-based systems, structurally based plumage produces bright colors
via constructive interference of light at the interfaces between
keratin, air and melanocytes in feather barbs and barbules (for a review, see
Prum, 1999
). As is the case
for most carotenoid-based ornamental displays, females generally prefer to
mate with males having the brightest structurally colored plumage ornaments
(Bennett et al., 1997
;
Andersson and Amundsen, 1997
;
Andersson et al., 1998
;
Hunt et al., 1999
). Moreover,
variability in structural coloration appears to be related to the nutritional
condition of males during molt (Keyser and Hill,
1999
,
2000
;
Doucet, 2002
). However, these
findings that point to a proximate mechanism underlying variation in
structural plumage ornaments are only correlational; as of yet, no experiments
have been conducted to assess the environmental or physiological factors that
affect the expression of structurally based color displays in birds.
Here we investigate the effect of nutritional constraints during molt on
the expression of both melanin-based and structurally based ornamental plumage
coloration. We studied these two forms of plumage coloration in two sexually
dichromatic songbird species: the house sparrow Passer domesticus and
the brown-headed cowbird Molothrus ater. Males of both species grow
colorful plumage in the fall through a pre-basic molt and display the ornament
throughout the year. Male house sparrows exhibit a melanin-based black throat
patch (Lowther and Cink,
1992), and male cowbirds have structurally based iridescent
green-black plumage coloration on the breast and back
(Lowther, 1993
). Male cowbirds
also possess a deep brown, melanin-based hood that extends down to the nape
and throat (Lowther, 1993
).
Female sparrows and cowbirds are drab brown in coloration.
The house sparrow is one of the best-studied of all songbird species in the
context of sexual selection, and certainly the most common subject in work on
melanin-based plumage. Males with larger black badges are behaviorally
dominant to males having smaller badges (Møller,
1987a,b
).
Males with the largest patches also experience the highest reproductive
success in most populations (Møller,
1988
,
1992
;
Veiga, 1993
; but see
Griffith et al., 1999
). In
contrast, little is known of the function of bright plumage in male
brown-headed cowbirds. Visual displays accompany courtship vocalizations prior
to mating (Lowther, 1993
), and
in other cowbird species the extent of sexual dichromatism is positively
associated with variance in male mating success
(Hauber et al., 1999
).
However, more work is needed to determine whether or not ornamental coloration
is a sexually selected trait in this species.
To test the hypothesis that the expression of melanin-based and
structurally based plumage coloration is dependent on nutritional condition in
male house sparrows and brown-headed cowbirds, we restricted access to food
during randomized time intervals for captive groups of treatment birds, while
allowing control males access ad libitum to the same diet throughout
the course of molt. We followed the experimental methods of Hill
(2000), who found that
nutritional stress has a significant impact on the brightness of
carotenoid-based plumage in male house finches Carpodacus mexicanus.
We housed captive cowbirds individually and sparrows in triads to minimize
pseudoreplication from housing all birds within a treatment group in the same
cage (e.g. Brawner et al.,
2000
; Hill, 2000
;
McGraw and Hill, 2000
). At the
end of molt, we compared the brightness of ornamental plumage between control
and experimental groups.
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Materials and methods |
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Brown-headed cowbirds
15 male cowbirds Molothrus ater Boddaert of known age were used in
this study, which spanned 2 years (2000 and 2001). In 2000, we housed ten
cowbirds in individual hardware cloth cages (0.6 m x 0.3 m x 0.4
m) in an indoor room (2.9m x 4m x 2.4m) that was separate from the
house sparrows. Eight of these birds were previously banded adults (mean=2.6
years, range=2-4) who were removed as nestlings from the nests of song
sparrows Melospiza melodia and eastern phoebes Sayornis
phoebe from 1997-1999 and hand-raised to independence in captivity
(Hauber et al., 2000). The
remaining two birds were juveniles that we captured from the wild in Tompkins
County, NY, USA using baited Potter traps in July 2000. In 2001, we housed
five juveniles in a free-flying indoor group that also were obtained as
nestlings from phoebe nests. All of these males were part of a behavioral
study during the year in which they hatched
(Hauber et al., 2000
), but
were never manipulated physiologically or nutritionally prior to this
experiment. All other housing conditions follow those described above for
house sparrows.
General procedures
Before birds began molting in captivity, we quantified the melanin- and
structurally based ornamental plumage coloration that males displayed prior to
the experiment. We scored males from each species with an Ocean Optics, Inc.
S2000 fiber-optic spectrometer (Dunedin, FL, USA) illuminated by a
tungstenhalogen/deuterium light source (Analytical Instrument Systems,
Inc., Flemington, NJ, USA) to determine the degree to which both ornament
types reflected in the ultraviolet (for detailed methods, see
McGraw et al., 1999). Neither
the melanin pigmentation of male house sparrow badges and cowbird hoods nor
the iridescent plumage of male cowbirds exhibited a UV reflectance peak
(Fig. 1). Consequently, we
quantified only the visible light reflectance from the plumage of all males,
which should serve as a reliable assay of short-, medium- and long-wave light
reflectance, despite the fact that it may not truly capture what the birds see
(Cuthill et al., 2000
).
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To score house sparrow plumage, we digitally photographed the ventral
sections of each male against a grayboard (at an image resolution of
1760x1168 pixels) and imported these images into Adobe®
Photoshop® (Adobe Systems Inc., San Jose, CA, USA). We measured badge size
by outlining the melanin-based pigmented area using the `lasso' marquee and
determining the number of pixels occupied with the `histogram' function
(sensu Dale, 2000).
Although freshly molted badges are partially concealed by buff feather tips, a
number of studies have shown that measuring the area of black-pigmented
feathers from the base of the bill to the lowest point on the breast to which
black feathers extend is a reliable and meaningful scoring method
(Møller and Erritzøe,
1992
; Gonzalez et al.,
1999
; Griffith et al.,
1999
). Because photos may have differed slightly in distance from
the subject, badge area (in cm2) was calculated relative to an area
standard that was photographed next to each bird. We measured melaninbased
coloration as the brightness (also known as lightness or tone) of the badge at
its center using the `HSB scale' on Photoshop's `color picker' function. To
control for any lighting differences among photos, we scored badge brightness
as a percentage relative to a standard black color chip that also was
photographed with each male. Repeatability of both badge size and brightness,
as measured using separate photographs of the same birds, was high using these
scoring methods (area: r=0.91, F22,23=20.67,
P<0.0001; brightness: r=0.81,
F22,23=9.25, P<0.0001;
Lessells and Boag, 1987
).
We scored the color of cowbird plumage with a hand-held ColortronTM
reflectance spectrophotometer (Light Source Inc., San Rafael, CA, USA;
Hill, 1998). Although this
unit does not gather UV-reflectance data, it does quantify spectral
reflectance from 390-700 nm and derives tristimulus scores (hue, saturation
and brightness, using the ColorshopTM 2.6 software package) from the
generated reflectance curves (Light
Source, 1996
). Thus, as in other studies of avian structural
coloration (e.g. Andersson
1999
; Keyser and Hill,
1999
), hue represents the wavelength at maximum reflectance, for
which ColorshopTM assigns numerical values around a 360° color wheel
(with red starting at 0°). In this cowbird species with dark green-black
plumage, higher hue values correspond to shorter wavelengths of light (toward
blue/violet light). Saturation captures spectral purity and is measured by
ColorshopTM as a percentage relative to black and white standards
provided by Light Source Inc. (100%=fully saturated, or comprised entirely of
one light-wavelength). Lastly, brightness is a measure of the total amount of
light reflected by a surface (or area under the spectral curve), and again is
represented by ColorshopTM as a percentage (with 100% being total
reflectance, or white). For all measurements, the ColortronTM was held
perpendicular to the reading surface and the foot lever containing the 9
mm2 reading area depressed firmly against the feather patches. We
measured the hue, saturation and brightness of six colorful body regions
(upper, middle and lower portions of both the dorsum and venter) and averaged
these values to obtain mean hue, saturation and brightness scores for each
bird. All three color variables were moderately to highly repeatable using
this method (hue: r=0.93, F9,10=29.9,
P<0.0001; saturation: r=0.94,
F9,10=30.3, P<0.0001; brightness:
r=0.71, F9,10=5.96, P=0.01). We
quantified the color of melanin-based hoods in cowbirds by taking four
brightness measurements, on the top, back and two sides of the head, with the
ColortronTM and averaging these values to obtain a mean brightness score
for each male. Because male cowbirds also vary in the extent to which the
brown hood extends down the neck, we measured the length of the melanin patch
to the nearest 0.1 mm with digital calipers. Scoring the extent
(r=0.89, F9,10=26.8, P<0.001) and
brightness of melanin plumage (r=0.97,
F9,10=66.5, P<0.0001) was also highly
repeatable.
Prior to and during the experiment, captive males from both species were
fed ad libitum a 50:50 diet of unmedicated game starter (26% protein,
Agway® Inc., Batavia, NY, USA) and white millet. Water was treated with
6.6 drops l-1 of Premium Multi-DropsTM high-potency
multivitamins (Eight in One® Pet Products, Inc., Hauppauge, NY, USA) and
0.26 gl-1 of sulfadimethoxine (Sigma® Chemicals, St Louis, MO,
USA), a drug that effectively controls coccidial endoparasitism in these and
other passerine species (Brawner et al.,
2000; Hill, 2000
;
McGraw and Hill, 2000
).
Throughout our study, one food dish and one water dish were provided for each
bird, and spaced evenly on the floor of the sparrow cages, to ensure that all
individuals had equal access. At no point were any males infected with obvious
ectoparasites (e.g. ticks, avian pox, feather mites/lice).
The pre-basic molt period spans the late summer and fall for both species
(Lowther and Cink, 1992;
Lowther, 1993
), so we ran our
food-deprivation experiments from 15 July until all birds completed molt by 15
October. Following the protocol developed by Hill
(2000
), we removed the food
dishes from experimental groups for randomly selected 6 h periods of daylight
(a range of 42-52% of total daylight hours throughout the study) on 3 out of
every 4 days during molt. This randomized design was used to prevent birds
from tracking food removal and ingesting large quantities of food prior to
deprivation periods. As Hill
(2000
) found with house
finches, food-stressed cowbirds and sparrows were noticeably hungry after the
food-stress period and would descend from their perches to the floor of the
cage to consume food while dishes were still being replaced elsewhere in the
room. For control groups, who had access ad libitum to the
aforementioned diet throughout the study, we inserted our hands into the cages
to raise and lower the dishes to provide similar levels of disturbance when
dishes were removed and replaced in food-stressed cages. With 14 cages of
house sparrows, we randomly assigned 7 to the food-deprived group and 7 as
controls (N=21 males in both groups). In our 2-year cowbird study, we
divided the 10 individually housed cowbirds in 2000 into 5 treatment birds and
5 control birds (with one juvenile in each group), whereas in 2001 all 5 birds
were in the control group.
To ensure that food-deprived males consumed less food than did unstressed individuals, we measured food intake on 5 separate days during molt for house sparrows. At the start of the stress period on these days, we removed all old food from the dishes and provided 10 g dish-1 of fresh millet to each control cage. Food was available in the normal dishes, but these were placed inside larger containers that prevented birds from spilling seed out of the cage. In nutritionally deprived cages, dishes were empty to start and the same amount of millet was added after the 6 h deprivation period; control birds were similarly disturbed at this time. 24 h after the start of the stress period, we measured the amount of food consumed by each group using an electronic balance. Birds in both groups never consumed more than half of the seed that we provided during these trials, indicating that food intake reflected the feeding capacity of the birds rather than the gross quantity of millet available. We used non-parametric MannWhitney U-tests to analyze food intake data because of small sample sizes (7 cages per day per treatment group) and because not all variables were normally distributed (ShapiroWilk W-tests, P<0.05).
Once all males had completed their prebasic molt, we again measured the
body mass of each bird and quantified melanin-and structurally based
ornamental plumage coloration, following the protocols listed previously. We
also measured tarsus length for all cowbirds because it had not been
determined before the experiment. As a measure of nutritional stress on
feather growth and to ensure that treatment males were more stressed than
control birds, we plucked all six pairs of tail feathers from each sparrow at
the end of molt and measured the fluctuating asymmetry of rectrices with
calipers to the nearest 0.1 mm (sensu
Swaddle and Witter, 1994).
Rectrix-length measurements were highly repeatable (r=0.997,
F=749.7, P<0.0001) for a random subset of feathers
(N=25) measured twice (on 4 March and 8 October 2001), and
differences in tail symmetry (1.05±0.14%) far exceeded measurement
error (0.19±0.03%).
Statistical analyses
All analyses were performed using the statistical program StatView®
5.0.1 (SAS Institute 1998). To comprehensively analyze the predictors of
plumage color in our study, we used both univariate and multivariate
statistical procedures. We tested for normality (ShapiroWilk
W-test) and equality of variance (Equality-of-variances
F-test) in house sparrow data and used univariate, unpaired
t-tests when these assumptions of parametric statistics were met;
when assumptions were violated, we used non-parametric MannWhitney
U-tests. Because of small sample sizes, we used MannWhitney
tests in all cowbird analyses. We used analyses of covariance (ANCOVA) to
investigate the effect of nutritional stress on plumage expression; tarsus
length, body mass and pre-molt plumage scores were entered as covariates in
the models, and we added year and age into cowbird analyses. All data for
house sparrows were analyzed using both individual birds and individual cages
as units of analysis.
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Results |
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Plumage expression and nutritional condition in house sparrows
Prior to the experiment, there were no significant differences between
nutritionally deprived and undeprived sparrows in tarsus length (per
individual: U=155.5, P=0.16; per cage: U=39,
P=0.07) or body mass (individuals: U=166, P=0.17;
cages: U=34, P=0.22), nor were there initial differences in
the size (individuals: t=0.54, P=0.60; cages: U=22,
P=0.75) or brightness (individuals: t=0.74, P=0.46;
cages: U=19, P=0.48) of melanin-based throat badges
(Table 1). We found that
food-unlimited birds did not gain significantly more mass during the
experiment than did food-limited birds (individuals: U=170,
P=0.20; cages: U=34, P=0.22;
Table 1). Overall,
nutritionally stressed sparrows grew plumage badges that did not differ in
size or brightness from those of nutritionally unstressed birds
(Fig. 2; using cage means for
area: U=21, P=0.65; using cage means for brightness:
U=16.5, P=0.30). Using ANCOVA, we also found no effects of
nutritional deprivation, tarsus length, body mass or pre-molt badge area on
either badge size (all P>0.2 for both per-individual and per-cage
analyses) or badge brightness (all P>0.1).
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Because of these non-significant results, we evaluated the statistical
power of our tests by considering the likelihood of detecting results similar
to those for species in which a significant effect of food stress on plumage
color expression had been previously established. Hill's experiments with
house finches used sample sizes (N=7-13 per treatment) that were
smaller than those in our studies, but found much higher effects
(r2=0.33) than those for house sparrows in the present
study (all r2<0.07)
(Hill, 2000). With
N=21 in each experimental group, we had the statistical power to
detect effects
0.6 at
=0.05
(Cohen, 1988
). Thus, the
development of melanin-based ornamental coloration in house sparrows appears
to be much less sensitive to nutritional deprivation than is carotenoid
pigmentation in house finches.
Plumage expression and nutritional condition in brown-headed
cowbirds
Within the control group, juvenile males did not differ significantly from
adults in either melanin- (hood size: U=5, P=0.43;
brightness: U=3.5, P=0.24) or structurally based plumage
coloration (hue: U=18, P=0.45; saturation: U=21,
P=0.42; brightness: U=15.5, P=0.16), nor was there
any effect of year on our measures of ornamental color (all
P<0.25). Thus, we pooled birds across age classes and years for
analysis. Before the experiment, we found no significant differences in tarsus
length (U=9.5, P=0.53;
Table 1) between nutritionally
stressed and unstressed birds, nor were there initial differences between
treatment groups in the size (U=3.5, P=0.25) or brightness
(U=7, P=0.77) of the melanin-based brown hood, or in the hue
(U=5, P=0.37), saturation (U=7, P=0.77),
or brightness (U=7.5, P=0.88) of structurally colored
plumage (Table 1). Food-limited
birds did not differ in body mass from food-unlimited birds after the
experiment (U=12, P=0.92;
Table 1). Thus, for both
sparrows and cowbirds, and as Hill
(2000) found for house
finches, this food-deprivation protocol did not impose unreasonably high
levels of nutritional stress on the animals.
We detected no significant effect of nutritional stress during molt on the size and brightness of the melanin-based brown hoods (Fig. 3). However, in these same birds, nutritionally deprived males grew significantly less green, less saturated, and less bright iridescent plumage than did undeprived birds (Fig. 4). These results are consistent if we exclude all birds from 2001 (hue: U=5, P=0.10; saturation: U=1, P=0.02; brightness: U=1, P=0.01) and if we exclude all juveniles from the analyses (hue: U=0, P=0.02; saturation: U=1, P=0.04; brightness: U=0.5, P=0.03). ANCOVA results again supported those from univariate analyses. Neither treatment nor any of the covariates (year, age, tarsus, mass and pre-molt color) significantly predicted melanin-based hood size (all P>0.3) or brightness (all P>0.25). However, food-limitation did have a significant main effect on the hue, saturation, and brightness (all P<0.05) of iridescent coloration in male cowbirds (all other P>0.15).
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As with house sparrows, effect sizes for melanin color in cowbirds were
very low (r2=0.01). We had the power to detect effects up
to r2=0.35 in this experiment
(Cohen, 1988), even with our
small sample sizes. All of the significant effects for structural color were
large in this study (r2=0.65), but we encourage the use of
more birds in future studies to detect weaker effects. It is also worth
pointing out that, although iridescent plumage reflects light differently at
different incident angles, this color difference was detectable in our study
by measuring feather reflectance at only one angle (90° from surface) with
the ColortronTM.
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Discussion |
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Although certain correlative studies have linked melanin ornaments to
condition (e.g. Slagsvold and Lifjeld,
1988; Veiga and Puerta,
1996
), our data are consistent with more recent experimental
studies on the physiological constraints of melanin-based plumage ornaments.
Gonzalez et al. (1999
)
manipulated protein content in the diet of molting male house sparrows and
failed to detect any influence on the development of badge size and color.
McGraw and Hill (2000
) studied
the effects of coccidial infections on plumage displays in male American
goldfinches Carduelis tristis, and, despite significant effects of
endoparasitism on carotenoid-based ornamentation, found no differences in
melanin pigmentation between infected and uninfected birds. Why might the
expression of melanin coloration be uncoupled from the nutritional state of an
animal? The amino acid tyrosine serves as the precursor to the production of
melanin granules that are deposited in feathers
(Fox, 1976
). Although tyrosine
can be obtained in the diet through protein degradation or direct uptake, it
is a nutritionally dispensable (non-essential) amino acid
(Meister, 1965
), and can be
synthesized de novo from phenylalanine as long as there is organic
nitrogen in the diet (Moldawer et al.,
1983
). Thus, it seems that producing melanin pigments should not
be especially demanding energetically for birds.
Other physiological factors may be more likely to control the expression of
melanin-based ornamental coloration. Central to melanin production is
increased activity of the enzyme tyrosinase that acts at the cellular
organelles (melanosomes) of the epidermal melanocytes (color-producing cells)
(Fitzpatrick and Kukita,
1959). Certain hormones (e.g. estradiol, luteinizing-hormone) are
known to have stimulatory effects on tyrosinase activity and subsequent
biosynthesis of melanin granules in feather tracts (Hall,
1966
,
1969
;
Ralph, 1969
). Evans et al.
(2000
) and Gonzalez et al.
(2001
) recently found that
experimentally elevated levels of circulating testosterone increased the size
of the melanin badge in house sparrows. Testosterone also influences
aggressive behavior in birds (Wingfield et
al., 1987
), and thus may represent the proximate means by which
melanin ornaments can accurately signal social dominance and competitive
ability in animals.
To our knowledge, our investigation and documentation of the nutritional
condition-dependence of structurally based ornamental coloration is the first
experiment of its kind in any avian species. Fitzstephens and Getty
(2000) recently manipulated
the diet of male black-winged damselflies Calopteryx maculata who,
like male brown-headed cowbirds, display striking glossy green-black
coloration, and found that nutritionally deprived males were less colorful
than males provided with more food. Keyser and Hill
(1999
) detected a correlation
between the rate at which male blue grosbeaks Guiraca caerulea grew
tail feathers in the wild and the blueness of their structurally based
ornamental plumage. Doucet
(2002
) also observed a
positive relationship between feather growth and structural plumage coloration
in blue-black grassquits Volatinia jacarina from Mexico.
The relationship between structurally based ornamental coloration and
nutritional condition reported here is much like that found for
carotenoid-based ornamentation (Hill,
2000). Although based on only a few observations for structural
colors, both signals most often relay the condition of males during the time
at which the ornament is developed (e.g.
Hill, 1999
;
Keyser and Hill, 1999
; but see
Dale, 2000
) and are used in
female mate choice (e.g. Hill,
1999
; Hunt et al.,
1999
; but see Pryke et al.,
2001
). However, the means by which structural coloration is
produced is very different from that of carotenoid pigmentation.
Carotenoid-based colors have a direct tie to nutrition because vertebrates
must ingest these pigments through the diet to become colorful
(Brush, 1978
). In contrast,
structural colors in animals are produced by the physical interaction of light
with biological tissues (Fox,
1976
). Cowbirds produce perhaps the most simple of structural
colors, different from other previously studied species exhibiting structural
coloration (e.g. blue grosbeak), but much like starlings (Family Sturnidae)
and other birds with iridescent plumage. Their glossy, green-black sheen is
generated by the interference of light scattered by the keratin at the surface
of the feather and a single layer of melanin granules below
(Durrer, 1986
;
Prum, 1999
). So why might this
form of structurally based coloration, which contains melanin pigments, be
affected by an individual's nutritional condition?
Recent studies of plumage ultrastructure indicate that structurally colored
feathers are composed of highly organized matrices of keratin, air and
pigments, such that nanoscale variation in the orientation of melanin granules
or the uniformity and thickness of the tissue matrix may all contribute to the
directionality and intensity of light reflected (Prum et al.,
1998,
1999
; Andersson,
1999
,
2000
). Thus, in this case, fine
control over tissue and pigment arrangement during feather growth may be
particularly sensitive to perturbations in a bird's health or condition. As
there are a number of types of structural color in animals, depending on the
type (e.g. feathers, scales, skin, eye) and composition (amount and
arrangement of keratin, air and melanin) of the reflectance medium as well as
the type of light scattering (incoherent versus coherent;
Prum, 1999
), careful
examination of the potential condition-dependence for each of these forms is
warranted.
Although we have identified a link between nutrition and a form of
structurally based plumage ornamentation in this study, it will be important
in future research to investigate the full signal content of structural
coloration in brown-headed cowbirds and other species displaying this ornament
type. First, it is not known to what degree hormones may influence the
expression of structurally colored ornaments. Testosterone affects the speed
of acquiring structurally based breeding plumage in male superb fairy wrens
Malurus cyaneus (Peters et al.,
2000) and satin bowerbirds Ptilonorhynchus violaceus
(Collis and Borgia, 1992
,
1993
). However, much as for
melanin pigmentation, it is unclear if individual differences in plumage
brightness reflect variation in circulating androgens during molt per
se. Similarly, it is uncertain whether structural colors function in
male/male competitive situations as well as in female mate-attraction. As of
yet, no test of the status-signaling hypothesis has been conducted for
structurally colored ornaments in birds.
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Acknowledgments |
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References |
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