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EFFECTS OF DIET ON PLUMAGE COLORATION AND CAROTENOID
DEPOSITION IN RED AND YELLOW DOMESTIC CANARIES
(SERINUS CANARIA)
REBECCA E. KOCH,
1,3
KEVIN J. MCGRAW,
2
AND GEOFFREY E. HILL
1
ABSTRACT.—Atlantic Canaries (Serinus canaria) are the most commonly kept caged bird with extensive carotenoid-
based plumage coloration. Domestic strains of canaries have been bred for a variety of colors and patterns, making
them a valuable model for studies of the genetic bases for feather pigmentation. However, no detailed account has been
published on feather pigments of the various strains of this species, particularly in relation to dietary pigments available
during molt. Moreover, in the twentieth century, aviculturists created a red canary by crossing Atlantic Canaries with Red
Siskins (Carduelis cucullata). This “red-factor” canary is reputed to metabolically transform yellow dietary pigments into
red ketocarotenoids, but such metabolic capacity has yet to be documented in controlled experiments. We fed molting
yellow and red-factor canaries seed diets supplemented with either b-carotene, lutein/zeaxanthin, or b-cryptoxanthin/
b-carotene and measured the coloration and carotenoid content of newly grown feathers. On all diets, yellow canaries grew
yellow feathers and red canaries grew orange or red feathers. Yellow canaries deposited dietary pigments and metabolically
derived canary xanthophylls into feathers. Red-factor canaries deposited the same plumage carotenoids as yellow canaries,
but also deposited red ketocarotenoids. Red-factor canaries deposited higher total amounts of carotenoids than yellow
canaries, but otherwise there was little effect of dietary supplementation on feather carotenoid content, hue, or chroma.
These observations indicate that canaries can use a variety of dietary precursors to produce plumage coloration and that
red canaries can metabolically convert yellow dietary carotenoids into red ketocarotenoids. Received 4 September 2015.
Accepted 7 November 2015.
Key words: carotenoid conversion, carotenoid pigments, domestic canary, plumage coloration.
In most birds, red, orange, and yellow plumage
coloration is produced by carotenoid pigments
(Goodwin 1984, McGraw 2006). No birds can
synthesize carotenoids de novo, but some birds
can biochemically modify the carotenoids that
they ingest (Brush 1981). The main carotenoids
in the diets of most birds are lutein, zeaxanthin,
b-carotene, and b-cryptoxanthin, and some birds
convert these dietary pigments into yellow canary
xanthophylls or red ketocarotenoids (carotenoids
containing a ketone group) that they deposit into
feathers or bare parts (McGraw 2006). Although
these metabolic transformations have been deduced
for a handful of birds (Brush 1990, McGraw 2006),
such data are surprisingly lacking for Atlantic
Canaries (Serinus canaria), the most commonly
kept caged birds with extensive carotenoid plum-
age coloration.
In the wild on the Canary Islands, Atlantic
Canaries have yellow feathers on their heads and
breasts, with mostly brown wing, tail, and dorsal
plumage (Collar et al. 2010). This appearance
is retained in some domestic canary varieties,
particularly those bred for singing ability. In the
so-called “color-bred canaries,” however, a fantas-
tic range of color patterns and novel shades of
red, orange, and yellow have been generated
through selective breeding (Walker and Avon
1993, Birkhead 2003). In this study of feather
pigments, we focus on the relatively simple
lipochrome canaries, which have bright caroten-
oid-based coloration distributed more-or-less uni-
formly across the plumage with little or no melanin
pigmentation of feathers (Walker and Avon 1993).
Yellow lipochrome canaries have uniform bright
yellow coloration across their plumage; red-factor
lipochrome canaries, which originated in the early
1900s by crossing yellow lipochrome canaries with
Red Siskins (Carduelis cucullata; Birkhead 2003,
2014), have uniform red coloration across their
plumage. Although red-factor canaries originated
as a hybrid taxon, the hybrid offspring were
back-crossed with canaries with each generation
selected for red coloration but no other siskin
characteristics (Birkhead 2003). Thus, individuals
of this breed retain no measureable remnants of
siskin phenotype except red plumage coloration.
Within the pet trade, canaries are often “color
fed” by adding high doses of carotenoid pigments
to the diet of molting birds to induce an especially
1
Department of Biological Sciences, 331 Funchess Hall,
Auburn University, Auburn, AL 36849, USA.
2
School of Life Sciences, Life Sciences C-wing Rm. 522,
Arizona State University, Tempe, AZ 85287, USA.
3
Corresponding author; e-mail: rek0005@auburn.edu
The Wilson Journal of Ornithology 128(2):328–333, 2016
328
brilliant plumage color. In fact, even yellow
lipochrome canaries may acquire an orange tint
upon consumption of a diet exceptionally high in
red ketocarotenoids, though only red-factors may
acquire truly red coloration (Birkhead 2003, 2014).
However, the diets of seed-eating songbirds like
canaries typically contain exclusively yellow or
orange pigments that must be converted into red
pigments for ornamental coloration (Hill 2006).
Isolating the red-factor canary’s ability to metab-
olize yellow dietary carotenoids into red carot-
enoids in the absence of color feeding is essential
to understanding the differences in carotenoid pro-
cessing between red and yellow canaries, and may
have important broader implications for under-
standing the control and evolution of red carot-
enoid metabolism in birds and other animals.
Canaries have been used extensively in ornitho-
logical research. They are model animals for
song and neurobiological research (Goldman and
Nottebohm 1983, Brenowitz and Beecher 2005),
and strains have been developed with genetic
knockouts for carotenoid pigmentation (white
canaries) as well as for color variants (red, yellow,
orange, frosted, dark red, etc.; Walker and Avon
1993). Canaries could serve as a model for studies
of the genetic bases for carotenoid plumage
coloration (Pointer et al. 2012, Walsh et al. 2012),
and a first step in this process is deducing
what feather pigments are produced from specific
dietary precursors. In the only published experi-
mental study of feather pigmentation in domestic
canaries, Brockmann and Vo¨lker (1934) detected
canary xanthophylls in the feathers of canaries held
on a seed diet, but the authors did not examine
the metabolic processes occurring within these
birds. Modern carotenoid analytical techniques
are needed to substantiate and build on the results
of this study, which was one of the first to
quantify carotenoid content in the feathers of any
bird.
Here, we assess the effect of diet on plumage
pigmentation in yellow and red-factor lipochrome
canaries by feeding red and yellow canaries dif-
ferent carotenoid-containing diets during plumage
molt and measuring the pigments deposited in
newly grown feathers. Our goal is to demonstrate,
under controlled experimental conditions, that red-
factor canaries can convert yellow dietary carot-
enoids into red plumage pigments and to determine
the range of dietary precursors from which canar-
ies can produce different metabolic plumage
pigments.
METHODS
All canaries were housed as pairs in 0.46 by
0.46 by 0.92 m cages illuminated with full-
spectrum lights set to the natural photoperiod of
Auburn, AL. Birds were fed a maintenance diet of
primarily canary seed (All Natural Canary Blend,
Jones Seed Company, Lawton, OK, USA), which
provides sufficient nutrition for canaries to molt
and to breed, but has low levels of yellow dietary
carotenoids (,20 mg/g total, primarily lutein
and b-carotene with low levels of zeaxanthin;
Brockmann and Vo¨lker 1934, Li and Beta 2012)
that are well below the supplemented levels (see
more below). Birds of both sexes were included in
the experiment, because domestic canaries are
sexually monochromatic (Koch and Hill 2015).
In July 2014, we randomly divided 18 red-factor
and 18 yellow color-bred lipochrome canaries
(The Canary’s Nest, Virginia Beach, VA, USA),
evenly split between both sexes, equally into three
treatment groups that were supplemented with dif-
ferent yellow-orange dietary carotenoids: lutein/
zeaxanthin (FloraGLO, Kemin Industries Inc., Des
Moines, IA, USA), b-carotene (b-Carotene 15,
General Nutrition Centers Inc., Pittsburgh, PA,
USA), or ground freeze-dried papaya (Freshlydried,
Jersey City, NJ, USA). Papaya was used as
a source of b-cryptoxanthin, though it also pro-
vided birds with some b-carotene; papaya has about
four times the concentration of b-cryptoxanthin as
b-carotene (Chandrika et al. 2003). We chose these
supplementation regimens because they provided
birds with all four common carotenoids in the diets
of songbirds, with each of the four dietary
carotenoids supplied in abundance in at least one
dietary treatment. Three birds in the lutein/zea-
xanthin treatment died just after the start of
supplementation, so our final sample sizes were 4
red and 5 yellow in the lutein/zeaxanthin treatment,
6redand6yellowintheb-carotene treatment, and 6
red and 6 yellow in the papaya treatment.
Carotenoids for all treatments were applied as
powder to seed by adding about 3 g carotenoids to
20 g of canary seed. This method was designed
such that the levels of supplemented carotenoids
far exceeded the low levels of carotenoids present
in the seed diet, though we had no way to determine
exact carotenoid ingestion amounts per bird per
day. However, our methods were sufficient for the
goals of this study: to determine whether red or
yellow canaries have the physiological capability
to convert dietary yellow carotenoids to red
Koch et al. NCANARY CAROTENOID PIGMENTS
329
ketocarotenoids, and to draw conclusions about
which dietary carotenoid are suitable precursors
for carotenoid conversion.
Birds received experimental supplementation
throughout the duration of their annual fall
molt, August through October 2014. We monitored
birds on a weekly basis for growing feathers, and
removed 6–10 newly grown breast feathers from
each bird for color measurement and carotenoid
analysis. We removed ingrowing feathers that
retained some vascularized tissue in the shaft
(indicative of a growing feather), but which had
largely emerged from the protective sheath,
exposing ,1 cm of mature feather. We stacked
feather samples on nonreflective black cardstock
paper and measured their color using an Ocean
Optics USB4000 spectrophotometer (Ocean Op-
tics Inc., Dunedin, FL, USA) and the OOIBase32
program according to standard color measurement
protocols (Saks et al. 2003). Briefly, the spectro-
photometer probe was calibrated against a white
(Labsphere Inc., North Sutton, NH, USA) and
dark standard, then was positioned ,5 mm from
the surface at a 90uangle for data collection.
A black rubber barrier blocked external light from
the sample; the surface was illuminated during
reflectance measurement with an Ocean Optics
PX-2 pulsed xenon light source. From the raw
reflectance spectra, we used the program CLR
(v. 1.05; Montgomerie 2008) to calculate one value
of hue (variable name H3) and one value of chroma
(also known as saturation; S3) for each individual;
we selected these variables because they have been
shown to most accurately reflect the carotenoid
content of feathers in another cardueline finch
that can display both red and yellow plumage,
the House Finch (Haemorhous mexicanus; Butler
et al. 2011).
We assessed the carotenoid content of each
bird’s feather sample using high-performance
liquid chromatography (HPLC) according to the
extraction and analysis methods described in
Toomey and McGraw (2010); individual carot-
enoids were identified based on external standard
curves run for each carotenoid. While our primary
goal was to qualitatively describe the types of
carotenoids present or absent within canaries of
each treatment and color type, we also used
analysis of variance (coupled with Tukey’s
Honest Significant Difference post-hoc tests),
t-tests, and linear regression models in R (version
3.0.2; R Core Team 2013) to investigate possible
quantitative relationships between diet treatment,
plumage color, and feather carotenoid concentra-
tions within red and yellow canaries.
RESULTS
Based on human visual categorization, all red-
factor canaries produced only orange and red
feathers (never yellow) and all yellow lipochrome
canaries produced only yellow feathers, regardless
of diet treatment. Yellow lipochrome canaries
deposited only yellow canary xanthophylls and
lutein into feathers, whereas red-factor canaries
deposited yellow canary xanthophylls, lutein, and
red ketocarotenoids into plumage (Table 1; Ap-
pendix). Thus, red but not yellow canaries were
able to produce red ketocarotenoids from both
carotene (carotenoids containing only carbon and
hydrogen; e.g., b-carotene) and hydroxycarote-
noid (carotenoids containing a hydroxyl group,
such as zeaxanthin) precursors (Fig. 1).
TABLE 1. Average carotenoid content (6SD) of feathers from red or yellow canaries on one of three supplemental
carotenoid treatments: b-carotene, lutein and zeaxanthin, or b-cryptoxanthin and b-carotene. All carotenoid measurements
are in units of mg carotenoids per g feather; hue is in units of nm, such that higher values indicate redder color; saturation is
a unitless ratio calculated from the feather reflectance spectra such that higher values indicate more saturated color.
“Yellow carotenoids” comprises lutein, canary xanthophylls A, B, and C, and xanthophyll isomers generated from these
pigments during extraction; “Red carotenoids” comprises echinenone, canthaxanthin, a-doradexanthin, and ketocarotenoid
isomers generated during extraction.
Color type Treatment Yellow carotenoids Red carotenoids Total carotenoids Hue Saturation
Red b-Carotene 222.8 682.5 367.6 6244.0 590.4 6296.4 441.8 6120.0 0.374 60.047
Lutein/zeax. 170.0 661.7 310.8 6391.2 480.8 6446.1 408.0 6103.6 0.368 60.021
b-Crypt./b-Carotene 185.3 699.0 121.3 667.8 306.6 6164.0 422.0 697.9 0.361 60.021
Yellow b-Carotene 170.1 697.1 0 170.1 697.1 330.6 629.4 0.337 60.021
Lutein/zeax. 229.2 6207.4 0 229.2 6207.4 364.2 625.1 0.324 60.021
b-Crypto./b-Carotene 320.3 6161.4 0 320.3 6161.4 386.5 663.7 0.340 60.026
330
THE WILSON JOURNAL OF ORNITHOLOGY NVol. 128, No. 2, June 2016
Red canaries had higher total feather carotenoid
concentration than yellow canaries across all treat-
ments (average difference between red and yellow 5
213.8 mg/g, F
1,27
56.84, P50.014; Table 1;
Fig. 2). However, there was no significant difference
in concentration of yellow plumage carotenoid
pigments between red and yellow canaries (average
difference between red and yellow 545.0 mg/g,
F
1,31
50.93, P50.34; Table 1), so differences in
total carotenoids appeared primarily because of the
extra presence of red carotenoids in their feathers.
There were no significant effects of diet treat-
ment on plumage hue, saturation, total carotenoid
concentration, total yellow carotenoid concentra-
tion, or total red carotenoid concentration (for red
canaries only; all P.0.16), with the exception
FIG. 1. Diagram illustrating the chemical structures and relevant conversion pathways of four dietary carotenoids
(lutein, zeaxanthin, b-cryptoxanthin, and b-carotene) into the metabolically altered carotenoids detected in canary feathers
(canary xanthophylls A, B, and C, echinenone, canthaxanthin, and a-doradexanthin). The letters above the arrows indicate
the nature of the reaction undergone: D 5dehydrogenation, H 5hydroxylation, and O 5oxidation (McGraw 2006).
FIG 2. The average total feather carotenoid concentration (6SD) in the feathers of yellow and red canaries fed one
of three supplemental carotenoid treatments: b-carotene, lutein and zeaxanthin, or b-cryptoxanthin and b-carotene.
Yellow and red canaries supplemented with b-carotene (designated by bracket) differed significantly in total carotenoid
concentration; all other comparisons among groups were nonsignificant.
Koch et al. NCANARY CAROTENOID PIGMENTS
331
that red-factor canaries on the b-carotene treat-
ment had significantly more total carotenoids than
yellow canaries on the same treatment (average
difference between red and yellow 5420.3 mg/g,
t53.30, df 56.06, P50.016; Table 1; Fig. 2).
However, we found that the total carotenoid con-
centration of canary feathers had a significant
positive correlation with plumage saturation
(slope 50.000096, F
1,30
528.2, P,0.001),
but not hue (slope 50.088, F
1,30
51.56, P5
0.13), in both color types. Saturation is therefore
a better predictor than hue of feather carotenoid
content in this species.
DISCUSSION
Wild-type canaries deposit canary xanthophylls
in their feathers to produce the species-typical
yellow feather coloration (Stradi 1999). In the
early twentieth century, aviculturists crossed
Atlantic Canaries with Red Siskins to produce
canaries capable of growing red feathers (Birkhead
2003, 2014), and all domestic canaries with red
plumage are descended from such siskin-canary
crosses (Walker and Avon 1993). Although the
techniques for genetically engineering red-factor
canaries are well known (Birkhead 2003, 2014),
the dietary basis and plumage pigment pathways
of red or yellow domestic canaries had not been
described (Stradi 1998, McGraw 2006). Thus, the
study presented here represents the first controlled
experimental test of the hypothesis that red
lipochrome canaries produce red ketocarotenoids
from yellow dietary pigments.
On any of the carotenoid-supplemented diets that
we provided, which varied from containing extra
xanthophylls (e.g., lutein/zeaxanthin, b-crypto-
xanthin) to carotenes (e.g., b-carotene), yellow
canaries deposited canary xanthophylls A, B, and C
as well as lutein in their feathers. Thus, regardless
of supplementation regimen, these birds could not
metabolize dietary pigments into red plumage
pigments. In addition, we found that red-factor
canaries can convert a diverse array of dietary
precursors—namely b-carotene, lutein/zeaxanthin,
and b-cryptoxanthin—into the red ketocarotenoids
a-doradexanthin, canthaxanthin, and echinenone.
These data are the first experimental demonstration
that red canaries can produce red ketocarotenoids
from yellow dietary precursors alone.
Because we did not carefully control the quan-
tities of carotenoids consumed by birds in our
experiments, comparisons of feather carotenoid
concentrations across diet treatments must be
considered cautiously. Nevertheless, the data
present some interesting patterns. When fed the
same diets, red canaries had significantly more
total carotenoids in their feathers than yellow
canaries. In contrast, red and yellow canaries did
not differ in yellow plumage carotenoid concen-
tration, so the difference in total feather caroten-
oid levels resulted from the addition of red
pigments to the yellow pigments present in both
canary strains. This observation implies that the
pathway for ketolation of red pigments in canaries
does not work from the end point of the pathway
for canary xanthophylls, in which case yellow
pigments would be depleted and would exist in
red birds in lower concentrations. Rather, it seems
that the red ketolation pathway runs in parallel to
the yellow hydroxylation pathway (Hill and
Johnson 2012). Parallel conversion pathways
likely explain our finding that in canary plumage,
carotenoid concentration predicts saturation but
not hue of feathers. Hue has been found to reflect
the ratio of red to yellow carotenoid pigments in
feathers of House Finches, which do not use
parallel conversion pathways (Inouye et al. 2001);
the lack of a relationship between carotenoid
pigment concentration and hue in the canary
indicates that the feathers contain a generally
uniform ratio of red and yellow pigments,
indicative of parallel conversion pathways.
Saturation, on the other hand, tends to reflect
the absolute concentrations of carotenoid pigments
in feathers (Hill and McGraw 2006).
None of the treatments resulted in significant
differences in total feather carotenoid concentra-
tions of either yellow or red birds, except for the
b-carotene treatment on which red birds had more
total carotenoids than yellow birds. It is likely the
lack of precision in carotenoid delivery veiled
differences in how various carotenoid precursors
were used to produce feather pigments, but our
results do show that a range of pigment precursors
can enable birds to reach the same display
endpoint. This study is the first to establish that
domestic red-factor, but not yellow, canaries can
metabolize yellow-orange dietary pigments into
red ketolated pigments.
ACKNOWLEDGMENTS
We would like to thank R. Montgomerie for development
of the CLR program. Several Auburn University under-
graduates and graduate students (A. Halasz, X.R. Franko)
helped with canary husbandry and supplementation. R.E.
Koch was supported by NSF GRFP throughout the project.
332
THE WILSON JOURNAL OF ORNITHOLOGY NVol. 128, No. 2, June 2016
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