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How to reduce the costs of ornaments without reducing their effectiveness? An example of a mechanism from carotenoid-based plumage

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Carotenoid-based ornaments are often considered to be honest indicators of individual quality assessed by potential mates. However, males can use a variety of strategies that minimize the amount of costly carotenoids used while retaining the effectiveness of color signaling. Birds could do this by altering pigment intake, metabolism, or its presentation to a potential signal receiver. Here, we propose a new mechanism of lowering the costs of carotenoid displays in birds: differential allocation of pigments within single feathers. We studied the coloration of the yellow terminal tail bands of rectrices of male Bohemian waxwings. Using reflectance spectrometry, we show that the two central rectrices are most intensively colored compared to other rectrices. More detailed analyses reveal that these differences result from feather-specific patterns of rectrices coloration. The outer feather vanes of the outermost rectrices are more intensively colored compared to the inner vanes. However, the central rectrices have equally colored vanes that are, on average, more intensively pigmented than the outermost rectrices. When the waxwing tail is folded, the outermost rectrices are covered by other feathers, except for the narrow, outer vane. Central rectrices, however, form the outermost layers which are not obscured by other tail feathers. Thus, the feather vanes that are the most visible to potential viewers are also the most pigmented. These results support the occurrence of a previously overlooked mechanism to reduce the costs of carotenoid-based ornaments: precise pigment distribution to maximize efficiency of signals within single feathers. Significance statement: Males of many bird species use bright carotenoid-based plumage coloration to attract females. These traits are physiologically expensive such that only individuals in prime condition can develop the most vivid colors. Males often "cheat" to obtain attractive appearances at lower costs. We showed that this goal could be achieved by differential deposition of pigments into the most conspicuous feather regions. Bohemian waxwing males have yellow tips on their rectrices of which the outer vanes are more brightly colored compared to the inner vanes. These inner feather vanes are usually covered by other feathers and are, thus, less visible to conspecifics. The only exception is the pair of central rectrices that are fully exposed, and both feather vanes are equally colored. In this species, males minimize the use of costly carotenoid pigments while maintaining elaborate ornamentation of plumage regions that are most visible to potential mates.
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ORIGINAL ARTICLE
How to reduce the costs of ornaments without reducing
their effectiveness? An example of a mechanism
from carotenoid-based plumage
Adrian Surmacki
1
&Anastazja Ragan
1
&Ziemowit Kosiński
1
&Marcin Tobółka
2
&
PawełPodkowa
1
Received: 1 December 2015 /Revised: 17 February 2016 / Accepted: 18 February 2016 / Published online: 29 February 2016
#The Author(s) 2016. This article is published with open access at Springerlink.com
Abstract
Carotenoid-based ornaments are often considered to be honest
indicators of individual quality assessed by potential mates.
However, males can use a variety of strategies that minimize
the amount of costly carotenoids used while retaining the ef-
fectiveness of color signaling. Birds could do this by altering
pigment intake, metabolism, or its presentation to a potential
signal receiver. Here, we propose a new mechanism of lower-
ing the costs of carotenoid displays in birds: differential allo-
cation of pigments within single feathers. We studied the col-
oration of the yellow terminal tail bands of rectrices of male
Bohemian waxwings. Using reflectance spectrometry, we
show that the two central rectrices are most intensively col-
ored compared to other rectrices. More detailed analyses re-
veal that these differences result from feather-specific patterns
of rectrices coloration. The outer feather vanes of the outer-
most rectrices are more intensively colored compared to the
inner vanes. However, the central rectrices have equally col-
ored vanes that are, on average, more intensively pigmented
than the outermost rectrices. When the waxwing tail is folded,
the outermost rectrices are covered by other feathers, except
for the narrow, outer vane. Central rectrices, however, form
the outermost layers which are not obscured by other tail
feathers. Thus, the feather vanes that are the most visible to
potential viewers are also the most pigmented. These results
support the occurrence of a previously overlooked mechanism
to reduce the costs of carotenoid-based ornaments: precise
pigment distribution to maximize efficiency of signals within
single feathers.
Significance statement
Males of many bird species use bright carotenoid-based plum-
age coloration to attract females. These traits are physiologi-
cally expensive such that only individuals in prime condition
can develop the most vivid colors. Males often Bcheat^to
obtain attractive appearances at lower costs. We showed that
this goal could be achieved by differential deposition of pig-
ments into the most conspicuous feather regions. Bohemian
waxwing males have yellow tips on their rectrices of which
the outer vanes are more brightly colored compared to the
inner vanes. These inner feather vanes are usually covered
by other feathers and are, thus, less visible to conspecifics.
The only exception is the pair of central rectrices that are fully
exposed, and both feather vanes are equally colored. In this
species, males minimize the use of costly carotenoid pigments
while maintaining elaborate ornamentation of plumage re-
gions that are most visible to potential mates.
Keywords Bombycilla garrulus .Courtship behavior .Color
expression .Individual condition .Male display .Sexual
secondary traits
Introduction
In many animal species, the evolution of showy secondary
sexual characters in males is thought to be driven mainly by
Communicated by K. McGraw
*Adrian Surmacki
adrian@amu.edu.pl
1
Department of Avian Biology and Ecology, Faculty of Biology,
Adam Mickiewicz University, Umultowska 89,
61-614 Poznań,Poland
2
Institute of Zoology, PoznańUniversity of Life Sciences, Wojska
Polskiego 71C, 60-625 Poznań, Poland
Behav Ecol Sociobiol (2016) 70:695700
DOI 10.1007/s00265-016-2090-6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
female choice (Andersson 1994;butseeexamplesof
intraspecific signal evolution of ornaments, e.g., Ninnes and
Andersson 2014;Ninnesetal.2015). These characters include
integument coloration (e.g., Kodric-Brown 1985;Hill1991),
behavioral displays (e.g., Barske et al. 2011), courtship vocal-
ization (e.g., Tomaszycki and Adkins-Regan 2005), morpho-
logical structures (Andersson 1982), and many others. The
central assumption of honest advertisement models of sexual
selection isthat ornaments are costly to produce (Zahavi 1975,
1977). Numerous studies have shown that when an animals
condition isreduced by environmental factors (e.g., nutritional
and oxidative stress, pathogens, or increased parental effort),
the quality of ornamentation subsequently decreases (Griffith
2000; Nowicki et al. 2004;Hill2006). However, tactics used
by males to reduce ornament production costs may weaken
the linkage between ornament quality and condition (Hill
1994; Badyaev 2004). This process should induce sexual con-
flict because females should seek cues that accurately reflect
male quality (Hill 1994).
Carotenoid plumage is an example of costly ornamenta-
tion, and males could benefit by expressing it at reduced costs.
Carotenoids are acquired solely through diet, and animals ex-
perience trade-offs between allocating pigments into the in-
tegument coloration versus toward other important physiolog-
ical functions, like cellular respiration (Hill 2006,2014). Hill
(1994) and Badyaev (2004) reviewed several strategies used
by males to reduce the cost of carotenoid-based ornaments.
These strategies can be divided intotwo classes. The first class
is associated with carotenoid acquisition and metabolism. For
example, males may adjust their diet to maximize carotenoid
intake during the time of ornamental plumage growth
(McPherson 1988) that could be accomplished by selectively
choosing carotenoid-rich food or a food containing caroten-
oids that can be directly deposited into ornaments (Badyaev
2004). Alternatively, birds can selectively metabolize only the
carotenoids that are used for pigmentation, a strategy observed
in flamingos (Phoenicopterus spp.), orioles (Icterus spp.), and
scarlet ibises (Endocimus ruber)(Hill1994;Badyaev2004
and papers cited therein). In the second strategy class, males
alter the expression of carotenoid ornaments by maximizing
the display of pigments (Hill 1993). For example, confining a
pigmented plumage area to a small patch can lead to an in-
crease in color intensity or feather structure can be modified
such that the coloration is displayed in the most efficient man-
ner (Hill 1994). Although examples of such mechanisms were
described decades ago (Hill 1994 and papers cited therein),
this process has yet to be quantitatively described.
We propose a new mechanism for lowering the costs of
carotenoid-based plumage displays in birds: males produce
more elaborate coloration on the feathers and feather parts that
should be the most visible to the signal receivers. We suggest
that reduced production costs could be obtained by uneven
incorporation of carotenoids over ornaments. Less
conspicuous ornament areas may receive less pigment that,
instead, may be used in important physiological processes like
immune defense and/or could be diverted to ornamentation of
the most visible ornament areas.
Our model species is the Bohemian waxwing (Bombycilla
garrulus), a species with multiple carotenoid-based orna-
ments: a yellow terminal tail band; yellow, oval spots on the
tips of the primary feathers; and red, waxy appendages on the
secondary feathers (Svensson 1992). Although these caroten-
oid ornaments occur in both sexes, males display larger ap-
pendages and yellow patches that are more intensively colored
(Svensson 1992). A clear dichromatism in carotenoid orna-
ments suggests that these traits could evolve as a result of
female mate choice in Bohemian waxwings. Female prefer-
ences for red appendages have been demonstrated in the close-
ly related species, cedar waxwing (Bombycilla cedrorum,
Mountjoy and Robertson 1988). Here, we focused on the yel-
low tail band of males that is pigmented with canary xantho-
phylls A and B (McGraw 2006).
Methods
To minimize observer bias, blinded methods were used during
material collection and subsequent measurements and analy-
ses. All birds were collected dead after collisions with build-
ings in Poznań, western Poland, in winters of 2004 and 2008.
Sex was determined by morphological features (Svensson
1992), and visual assessment of reproductive organs during
dissection and male age was determined by feather morphol-
ogy (Svensson 1992). In this study, we used 35 yearling
males. Thus, the plumage ornaments that we studied were
grown while the male was a juvenile (nestling or fledgling).
However, yearling Bohemian waxwings may breed and per-
form courtship displays similar to adults (Cramp 1998); it is
therefore reasonable to assume that their colorful feathers may
play a role in sexual selection. Before dissection, all 12 rectri-
ces were plucked and stored in plastic bags in the dark until
further measurements.
Reflectance measurements
We measured the reflectance of the distal tips of the yellow
rectrices using a USB4000 spectrometer connected to a pulsed
xenon lamp PX2 (Ocean Optics, Dunedin, FL, USA) with a
bi-furcated fiber optic measuring probe FCR-7UV200-2-
1.5x100 (Avantes, Apeldoorn, The Netherlands). The probe
was held at a 90° angle to the feather surface and illuminated
an area of ca. 1 mm in diameter. Before measuring the
feathers, we standardized measurements using a white stan-
dard (WS-1-SL, Labsphere, North Sutton, NH, USA) while
the dark standard was taken by turning off the light source and
covering the probe. Spectral measurements were expressed as
696 Behav Ecol Sociobiol (2016) 70:695700
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percent reflectance of light per wavelength in relation to a
white standard reflectance (100 %). We measured reflectance
of all 12 rectrices. We took six readings from the dorsal side of
yellow tip in each rectrix, including three readings per inner
and outer vane.
We processed all the spectral data using RCLR v0.9.28
software (Montgomerie 2008). For each individual, we calcu-
lated the carotenoid chroma ((R
450
R
700
)/R
700
;
Montgomerie 2008), which is a good predictor of carotenoid
content in yellow feathers (Peters et al. 2004). We transformed
chroma values into positive values that are intuitively more
appropriate; the higher values express a higher carotenoid
chroma. In the analyses of between-feather color variation,
we used a carotenoid chroma averaged for the entire dorsal
side of the vane. In remaining analyses, we used a carotenoid
chroma averaged separately for the inner and outer vane.
Statistical analysis
We used ANOVA for repeated measurements to test for dif-
ferences in the average carotenoid chroma between yellow
tips of all rectrices. In this case, 12 repeated measurements
were compared. We applied the same method to test for dif-
ferences in the coloration between the outer and inner feather
vanes in right outermost (R1) and right central (R6) rectrices.
In total, four repeated measurements were compared. In both
analyses, we used the Tukey honest significant difference
(HSD) test for post hoc comparisons.
Results
There were significant differences in the carotenoid chroma
between rectrices within the same individual (F
11, 374
=7.62,
p< 0.001; Fig. 1). Post hoc tests revealed that both central
rectrices (i.e., L6 and R6) exhibited a significantly greater
carotenoid chroma compared to all others (Table 1); however,
the differences between L2 and R6 were only marginally sig-
nificant (Table 1). There were no statistically significant dif-
ferences in the chroma between L6 and R6 rectrices and be-
tween all remaining rectrices (L1L5, R1R5; Table 1).
Carotenoid chroma differed significantly between feather
vanes (outer and inner) and amongst rectrices (R1 and R6; F
3,
102
=23.25,p< 0.001; Figs. 2and 3). We found a significantly
greater carotenoid chroma in the outer vanes compared to the
inner vanes in the R1 rectrix (Tukey HSD test; p< 0.001;
Figs. 2and 3). In contrast, inner vanes and outer vanes were
equally chromatic in the R6 rectrix (Tukey HSD test; p=1.00;
Figs. 2and 3). The carotenoid chroma of the outer and inner
vanes of the R6 rectrix was significantly higher when com-
pared to the inner vanes of the R1 rectrix (Tukey HSD test;
p< 0.001 in both cases; Figs. 2and 3), but no differences were
0.64
0.66
0.68
0.70
0.72
0.74
0.76
0.78
0.80
0.82
Carotenoid chroma [arc sin]
Fig. 1 Carotenoid chroma of the yellow tips of the rectrices of yearling
male Bohemian waxwings (mean ± 95 % CF). Symbols on the x-axis refer
to rectrices on the left (L) and right (R) sides of the tail. Rectrices 1 and 6
are the outermost and innermost tail feathers, respectively
Tabl e 1 Results of Tukey HSD
tests comparing values of
carotenoid chroma of the yellow
tips of the rectrices of yearling
male Bohemian waxwings
RectrixL2L3 L4L5L6R6R5R4R3R2R1
L1 0.657 0. 796 1.000 0.888 ** ** 0.998 0.988 0.999 0.999 1.000
L2 1.000 0.977 1.000 * 0.054 1.000 1.000 0.993 0.990 0.431
L3 0.994 1.000 * * 0.999 1.000 0.999 0.998 0.586
L4 0.999 ** ** 1.000 1.000 1.000 1.000 0.997
L5 ** * 1.000 1.000 1.000 1.000 0.715
L6 1.000**********
R6 ** * ** ** **
R5 1.000 1.000 1.000 0.983
R4 1.000 1.000 0.930
R3 1.000 0.987
R2 0.991
For explanations of symbols, see Fig. 1. Values in each cell are pvalues for a given pair of comparisons
**p<0.001;*p<0.05
Behav Ecol Sociobiol (2016) 70:695700 697
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found when compared to the outer vanes of the R1 rectrix
(Tukey HSD test; p=0.14 and p= 0.12, respectively; Figs. 2
and 3).
Discussion
Our results demonstrate that, within the same pigment orna-
ment, coloration is significantly differentiated between feather
types and feather vanes. Several lines of evidences suggest
that this differentiation could evolve as a consequence of an
evolutionary strategy to lower the costs of male ornament
production while simultaneously maintaining its efficiency
as a visual signal. Our study provides the first evidence of this
mechanism.
Both within- and between-feather differences in the carot-
enoid chroma in waxwing males could be explained by their
relative conspicuousness. When the tail is folded, the two
central rectrices (L6 and R6) form the outermost and uncov-
ered layer (Fig. 4). Except for the narrow strip of the outer
feather vane, the remaining rectrices (L1L5 and R1R5) are
covered by feathers (Fig. 4). We demonstrate that waxwing
males produce more elaborate color (richer carotenoid chro-
ma) on the outer feather vane that is more often visible. The
only exceptions are the two central rectrices (R6 and L6), but
these are always exposed to potential signal receivers. In this
case, both feather vanes are equally colored and are on aver-
age more saturated compared to the other rectrices. Some
features of Bohemian waxwing courtship behavior suggest
that females may assess male quality based on the character-
istics of the dorsal surface of the folded tail (Cramp 1998).
Paired birds perch very close to each other, and the male
assumes a generally horizontal position with the tail depressed
(Cramp 1998). Also, displaying males bend their closed tail
laterally toward the female (Cramp 1998).
Because our study is correlative, we cannot rule out other,
non-adaptive, explanations for the color pattern of waxwing
rectrices. Research on several other species, including cedar
waxwings, indicates that yellow, carotenoid-based coloration
is a product of both pigment deposition and feather micro-
structure (Shawkey and Hill 2005). It is therefore possible that
differences in Bohemian waxwing tail coloration could be, at
least partially, a by-product of keratin organization in barbs.
However, recent studies have revealed that carotenoid-based
coloration is more influenced by a variation in carotenoid
content than feather microstructure (Shawkey et al. 2006;
Jacot et al. 2010). Thus, a variation in feather structure prob-
ably does not explain differences in the coloration between
rectrices and their vanes in Bohemian waxwing males.
Another possible explanation of between-feather variation in
carotenoid chroma could be a differential rectrix growth rate
or (and) an order of rectrix growth. However, in nestling pas-
serines, rectrices grow simultaneously (Shirihai et al. 2010),
so their growth rate and growth sequence are unlikely to
0.60
0.62
0.64
0.66
0.68
0.70
0.72
0.74
0.76
0.78
0.80
0.82
Carotenoid chroma [arc sin]
Fig. 2 Carotenoid chroma of the outer and inner vanes of the yellow R1
and R6 rectrices of yearling male Bohemian waxwings. Filled square
outer vane; empty square inner vane
300 350 400 450 500 550 600 650 700
5
10
15
20
25
30
Reflectance [ %]
Fig. 3 Mean reflectance spectra of the yellow tips of the rectrices of male
Bohemian waxwing. The gray and black lines refer to R1 and R6 rectrix,
respectively. Solid and dashed lines refer to outer and inner feather vanes,
respectively
L6 R6
Fig. 4 A photograph showing the positions of the rectrices on the dorsal
side of the tails of Bohemian waxwings (the two central feathers (L6 and
R6) are labeled)
698 Behav Ecol Sociobiol (2016) 70:695700
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
explain differences in carotenoid coloration. Moreover, the
yellow spots cover only ca. 5 mm of the distal tip of the rectrix
(ca. 7 % of the total feather length). If growth rate varies
between feathers, it seems unlikely that the region of the feath-
er that erupts from feathers first would be affected.
Numerous studies have demonstrated that carotenoid-
based traits bear important condition-dependent costs for their
owners (reviewed in Hill 2006). Environmental agents like
access to dietary pigments, parasite infections, and nutritional
state are the most important factors influencing plumage col-
oration change in the subsequent molt (reviewed in Hill 2006).
Moreover, carotenoid-based nuptial plumage coloration can
be influenced by carotenoid or energy trade-offs associated
with the use of carotenoids to either produce ornaments or
aid in physiological processes (e.g., molt, Serra et al. 2007)
or behavioral activities (e.g., parental care, Hill 2002).
According to the most recent hypotheses, vital cellular pro-
cesses like mitochondrial respiration create a strong linkage
between expression of carotenoid-based colors and various
aspects of animal condition (Hill and Johnson 2012;
Johnson and Hill 2013;Hill2014). Not surprisingly, males
tend to reduce the costs of carotenoid color development with-
out sacrificing their attractiveness. Mechanisms based on
Bpigment presentation^in a feather are especially important
because they directly affect how females perceive the color
signal. One of tactics used by males is to concentrate pigments
into a small, but intensively colored, plumage area. The ex-
ample is the extent of ventral carotenoid-based coloration in
the griscomi subspecies of the house finch (Haemorhouse
mexicanus), which show more concentrated carotenoid pig-
ments in a smaller patch area compared other populations of
house finches (Hill 1993; Badyaev 2004). Other mechanisms
to maximize carotenoid ornament display are based on mod-
ifications of feather structure. Barbs containing pigments may
be laterally compressed, so their broad sides are oriented per-
pendicularly to the surface of the feather (Brush and Seifried
1968;Olson1970;Hudon1991). The function of this modi-
fication is to increase chroma and to shift hue toward longer
wavelengths (Brush and Seifried 1968;Olson1970;Hudon
1991). Furthermore, carotenoid-containing barbs have re-
duced barbules to enhance transmission of colored light
(Brush and Seifried 1968;Olson1970). This kind of
carotenoid-pigmented feather modification has been de-
scribed in several species, for example Gouldian finches
(Poephila gouldiae,BrushandSeifried1968), Guianan
cock-of-the-rock (Rupicola rupicola,Olson1970), and west-
ern tanager (Piranga ludoviciana,Hudon1991).
Compared to the above examples, the proposed mechanism
of carotenoid display maximization revealed in waxwing
males seems to be highly fine-tuned. It is based on a very
precise distribution of pigment within a small area of a single
feather. Moreover, the pattern of within-feather coloration de-
pends on the location of the feathers on the birds body. Birds
probably do not simply confine yellow coloration to the outer
feather vane of the one to five rectrices because inner feather
vanes are also sometimes visible, depending on the extent to
which the tail is spread.
Although yearling Bohemian waxwings breed and use
carotenoid-based ornaments during courtships (Cramp
1998), similar studies focusing on females and older males
are warranted. Considering that production of structural and
melanin-based colors may also be physiologically costly (e.g.,
Peters et al. 2007; Siefferman and Hill 2007;Galvánand
Solano 2015) and that, in many avian species, colorful orna-
ments are located on rectrices (e.g., greenfinch Chloris
chloris,Hõraketal.2004), the mechanism reported here
might be quite common and not restricted to carotenoid-
based coloration. The strategy of feather vane-specific pig-
ment investment could be easily tested in carotenoid supple-
mentation experiments. We would expect that individuals fac-
ing deficiency of pigments in their diet should locate them
more specifically in most visible feathers or feather parts. In
contrast, when carotenoids are abundant, the within-ornament
variance may be expected to be less extreme.
Acknowledgments We express our special gratitude to Lynn
Siefferman for the linguistic corrections and many comments that im-
proved the manuscript. We are grateful to Zbigniew Kwieciński
and Szymon Jędrzejewski for the assistance in processing the birds.
Matthew D. Shawkey provided helpful comments on the possible rela-
tionships between barb structure and light reflectance. We also thank Piotr
Zduniak and the two anonymous referees for their constructive comments
which shaped the final version of the manuscript.
Compliance with ethical standards All applicable international, na-
tional, and institutional guidelines for the care and use of animals were
followed. All animal procedures performed in this study were in accor-
dance with the ethical standards of Adam Mickiewcz University in
Poznań.
Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give appro-
priate credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
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