Can House Finches (Carpodacus mexicanus) use non-visual cues to discriminate the carotenoid content of foods?

Abstract

Carotenoid pigments are involved in different physiological processes (e.g., immunoenhancement, antioxidant activity) in addition to coloring plumage and integuments. As animals cannot synthesize these pigments de novo, it has been proposed that carotenoids constitute a limiting resource that birds may specifically seek in their food. Confirming this hypothesis, it was recently found that birds can discriminate between carotenoid-enriched diets and control diets, even if both have the same color, suggesting that there may be underlying non-visual (e.g., olfactory, taste) mechanisms for detecting carotenoid presence or enrichment in foods. In this study, we performed two experiments with male House Finches (Carpodacus mexicanus) to test if this species is able to discriminate between (1) carotenoid-enriched and plain sunflower seeds (while controlling for food coloration), and (2) plain seeds scented with β-ionone, which is a carotenoid-degradation product that is common in many fruits and is one of the most powerful flavor-active organic compounds, or a sham odorant. We found that finches did not show significant food preferences in either experiment, indicating that they did not use odor or flavor cues associated with carotenoids to discriminate between foods. However, our results do not rule out the possibilities that other flavors or odors can be used in discrimination or that finches may learn to discriminate flavors and odors over longer periods of time or at other times of year through post-ingestive feedback mechanisms.

Full text

ORIGINAL ARTICLE
Can House Finches (Carpodacus mexicanus) use non-visual cues
to discriminate the carotenoid content of foods?
Mathieu Giraudeau •Matthew B. Toomey •
Kevin J. McGraw
Received: 19 July 2011 / Revised: 20 November 2011 / Accepted: 15 January 2012 / Published online: 22 February 2012
ÓDt. Ornithologen-Gesellschaft e.V. 2012
Abstract Carotenoid pigments are involved in different
physiological processes (e.g., immunoenhancement, antioxi-
dant activity) in addition to coloring plumage and integuments.
As animals cannot synthesize these pigments de novo, it has
been proposed that carotenoids constitute a limiting resource
that birds may specifically seek in their food. Confirming this
hypothesis, it was recently found that birds can discriminate
between carotenoid-enriched diets and control diets, even if
both have the same color, suggesting that there may be
underlying non-visual (e.g., olfactory, taste) mechanisms for
detecting carotenoid presence or enrichment in foods. In this
study, we performed two experiments with male House Fin-
ches (Carpodacus mexicanus) to test if this species is able to
discriminate between (1) carotenoid-enriched and plain sun-
flower seeds (while controlling for food coloration), and (2)
plain seeds scented with b-ionone, which is a carotenoid-
degradation product that is common in many fruits and is one
of the most powerful flavor-active organic compounds, or a
sham odorant. We found that finches did not show significant
food preferences in either experiment, indicating that they did
not use odor or flavor cues associated with carotenoids to
discriminate between foods. However, our results do not rule
out the possibilities that other flavors or odors can be used in
discrimination or that finches may learn to discriminate flavors
and odors over longer periods of time or at other times of year
through post-ingestive feedback mechanisms.
Keywords Carotenoids Foraging Olfaction 
House Finch
Zusammenfassung
Ko
¨nnen Hausgimpel (Carpodacus mexicanus) andere als
optische Informationen verwenden, um den Karotinoid-
Gehalt ihrer Nahrung einzuscha
¨tzen?
U
¨ber die Farbgebung von Gefieder und Haut hinaus sind
Karotinoid-Farbstoffe an diversen physiologischen Pro-
zessen beteiligt (Sta
¨rkung des Immunsystems, Antioxidant-
ien-Aktivita
¨t). Da Tiere diese Farbstoffe nicht selbst
synthetisieren ko
¨nnen, wurde bereits die Idee pra
¨sentiert,
Karotinoide stellten einen Ressource-Faktor dar, den Vo
¨gel
gezielt in ihrer Nahrung suchen. Als Besta
¨tigung dieser
Hypothese wurde ku
¨rzlich herausgefunden, dass Vo
¨gel
zwischen Karotinoid-angereicherter und Kontroll-Nahrung
unterscheiden ko
¨nnen, auch wenn beide die gleiche Farbe
haben. Dies legt nahe, dass es außer optischen noch andere
Informationen geben muss (z. B. Geruch, Geschmack), die
als Mechanismen dienen ko
¨nnen, das Vorhandensein von,
und den Gehalt an, Karotinioden in der Nahrung festzu-
stellen. In unserer Untersuchung fu
¨hrten wir ein Zwei-Stu-
fen-Experiment mit ma
¨nnlichen Hausgimpeln (Carpodacus
mexicanus) durch, um zu testen, ob diese Art unterscheiden
kann zwischen (1) Karotinoid-angereicherten und reinen
Sonnenblumensamen (bei gleicher Farbe), und (2) reinen,
mit b-Iononen parfu
¨rmierten Samenko
¨rnern und solchen
Communicated by F. Bairlein.
Electronic supplementary material The online version of this
article (doi:10.1007/s10336-012-0829-z) contains supplementary
material, which is available to authorized users.
M. Giraudeau (&)M. B. Toomey K. J. McGraw
School of Life Sciences, Arizona State University,
Tempe, AZ 85287-4501, USA
e-mail: giraudeau.mathieu@gmail.com
Present Address:
M. B. Toomey
Department of Pathology and Immunology, Washington
University School of Medicine, St. Louis, MO 63110, USA
123
J Ornithol (2012) 153:1017–1023
DOI 10.1007/s10336-012-0829-z

mit einem anderen, a
¨hnlichen Duft (b-Ionone sind ein in
vielen Fru
¨chten vorkommendes Abbauprodukt von Karo-
tinoiden und eine der am sta
¨rksten duftenden organischen
Verbindungen u
¨berhaupt). Wir stellten fest, dass die Finken
in den Experimenten keinerlei signifikante Bevorzugung
einer der Nahrungsstoffe zeigten, was darauf hinwies, dass
sie in der Wahl ihrer Nahrung keine mit Karotinoiden zu-
sammenha
¨ngende Geschmacks- oder Geruchs-Informatio-
nen benutzten. Andererseits schließen unsere Ergebnisse
aber auch nicht die Mo
¨glichkeit aus, dass in der Unter-
scheidung von Nahrungsstoffen ein anderer Geruch oder
Geschmack benutzt wurde, oder dass die Finken die Un-
terscheidung anhand von Geruch oder Geschmack u
¨ber
einen la
¨ngeren Zeitraum oder zu anderen Jahreszeiten u
¨ber
Ru
¨ckkopplungsmechanismen in der Verdauung lernen.
Introduction
Most food items in nature offer animals a variety of
nutrient types and concentrations (Pulliam 1975). How-
ever, animals often need particular nutrients to meet
somatic or reproductive demands and in some instances
have developed foraging strategies to pursue food that
contains these specific limiting nutrients (Murphy and King
1987). Detection and discrimination of foods enriched with
calcium, sodium, or amino acids are widespread (e.g.,
Murphy and King 1987; Shulkin 1992; Tordoff 2001).
Carotenoids are valuable nutrients that have attracted
much research attention by behavioral ecologists in recent
years (Svensson and Wong 2011). Carotenoids generate the
yellow, orange, and red color of many animals (McGraw
2006) and are involved in different physiological pro-
cesses, such as immunomodulation, antioxidant activities,
and visual tuning (McGraw 2006). As animals cannot
synthesize these pigments de novo, it has been proposed
that carotenoids constitute a limiting resource for birds
(Blount 2004; Costantini et al. 2007), and have become a
model system for examining the costs and functions of
bright coloration (Blount and McGraw 2008).
Given the diverse benefits of carotenoids, natural
selection may favor the evolution of specific capacities to
detect food containing high levels of carotenoids (McGraw
2006; Senar et al. 2010). Color has been proposed as the
primary means of identifying carotenoid-rich foods
(McGraw 2006), but there are currently conflicting reports
in the literature on this mechanism. First, in a survey of 60
bird-dispersed fruiting tree species, Schaefer et al. (2008)
showed that fruit coloration was not linked with carotenoid
content. In contrast, a recent experimental study with Great
Tits (Parus major) found that birds are able to discriminate
between carotenoid-enriched diets and control diets, even if
both have the same color (Senar et al. 2010). Moreover,
Catoni et al. (2011) found that individual Garden Warblers
(Sylvia borin) did not select food for the maximum amount
of carotenoids, but choose for a highly consistent carot-
enoid intake during the course of different dual-choice
experiments where they had the choice between caroten-
oid-enriched and control diet, both with the same color.
Taken together, these results suggest that there may be
underlying non-visual (e.g., olfactory, taste) mechanisms
for detecting carotenoid presence/enrichment in foods.
To test this idea, we performed two captive experiments
with House Finches (Carpodacus mexicanus)—a North
American passerine species with sexually selected carot-
enoid-based male plumage coloration (Hill 2002). We
repeated Senar et al.’s (2010) experiment and offered males
a choice between carotenoid-enriched and plain sunflower
seeds, while controlling for food coloration by dyeing the
seeds green and presenting the food under filtered light.
Thus, this first experiment offered the birds the opportunity
to discriminate carotenoid content of food based on smell
or taste. In the second experiment, we isolated the olfactory
component by presenting the birds with a choice of plain
seeds scented with b-ionone or a sham odorant. b-ionone
was chosen because it is a product of carotenoid degrada-
tion, is common in many fruits, is a known attractant for
invertebrates, and is one of the most powerful flavor-active
organic compounds known (Britton 2008). We predict that
birds may prefer seeds scented with b-ionone if they dis-
criminate between foods using their smell. Finally, to
determine if the ability to detect carotenoids in food is
related to a male’s plumage carotenoid-based coloration,
we examined the link between food preference and plum-
age coloration in both experiments.
Methods
Study animals
From 1 September to 3 October 2010, we captured 15 male
House Finches using baited basket traps (McGraw et al.
2006) from each of three sites in the Phoenix metro area:
Estrella Mountain Regional Park, Goodyear, AZ (Site 1);
Arizona State University (ASU) Campus, Tempe, AZ (Site
2); and a private residence in Chandler, AZ (Site 3). Birds
were caught at the different sites as part of a separate
ongoing study of finches in different urban/rural settings.
We housed birds individually in small wire cages
(0.6 90.4 90.3 m) in an environmental chamber on the
ASU campus, at a constant temperature of 20°C and a
photoperiod that mimicked natural conditions. Birds were
fed an ad libitum diet of black oil sunflower seeds and tap
water.
1018 J Ornithol (2012) 153:1017–1023
123

Plumage coloration
Plumage coloration was quantified using digital photogra-
phy, following standard published methods for this species
(Oh and Badyaev 2006) and others (e.g., McGraw et al.
2002). Because House Finch plumage does not signifi-
cantly reflect in the UV (Keyser and Hill 1999; McGraw
and Hill 2000), techniques that rely on visible-light are
sufficient to capture variation in bird-visible and carot-
enoid-relevant coloration. Using a Canon PowerShot
SD1200S, we took two separate photographs of the head,
breast, and rump of each bird against a gray-board, using
identical distances from camera to object, shutter, expo-
sure, and flash settings for each photograph, and including
a color/size standard in each photo to control for any slight
variations in object illumination. Ambient lighting was
kept constant by photographing finches in the shade of
buildings. Digital images (JPEG, 3,648 92,736 pixels)
were imported into Adobe Photoshop to extract plumage
hue of the carotenoid coloration. Values for the two pic-
tures of each bird were averaged for statistical analyses
(repeatability =0.99 calculated using the method of Les-
sells and Boag 1987).
Carotenoid discrimination test
To examine whether House Finches can non-visually dis-
criminate foods on the basis of carotenoid content, we
prepared two types of experimental seed—control and
carotenoid-enriched. Control seed consisted of plain whole
sunflower seed kernels, which contain very low levels of
carotenoids (see below), while carotenoid-enriched seed
consisted of the same seeds coated with zeaxanthin
(OptiSharp
TM
; DSM, Heerlen, Netherlands). To apply the
carotenoid to the seed, we suspended 4.5 mg of zeaxanthin
in 150 ml of water, spread it over 450 g of seed, then dried
the seeds overnight at 50°C. This supplementation signif-
icantly enhanced the carotenoid content of the seeds
(t=9.62, df =2.45, p=0.0052). The high-carotenoid
seed contained 3.72 ±0.25 lg/g of total carotenoids,
while the regular seeds contained 1.21 ±0.08 lg/g. Both
concentrations are in the range of carotenoid concentra-
tions found in natural House Finch food (Hill et al. 2002).
In an effort to remove possible color-visual cues generated
by the addition of carotenoids (carotenoid-enriched seeds
were more orange), we dyed both seed types with 30 drops
of green food coloring (McCormick, Sparks, MD, USA), a
preferred food color of House Finches (Bascun
˜a
´n et al.
2009), and presented the seeds under filtered light. We
placed red filters (Roscolux Fire #19; Rosco Laboratories,
Stamford, CT, USA) over standard fluorescent light bulbs
(Sylvania, 34 W, T12 rapid start Super Saver; Osram-
Sylvania, Danvers, MA, USA) to produce a light envi-
ronment limited to wavelengths [550 nm (Toomey and
McGraw 2011). We measured the spectral properties of
both seed types with a UV–Vis spectrophotometer (Butler
et al. 2011), and assessed the chromatic and achromatic
contrast of the types using an avian visual model (Voro-
byev et al. 1998; supplemental methods). The spectral
sensitivities of the House Finch are not known, so we used
parameters from the Canary (Serinus canaria), the most
closely related species for which these data are available
(Das et al. 1999). We found that the carotenoid-enriched
seeds were visually indistinguishable from the control
seeds when all were dyed green and presented under red-
filtered light; in other words, the avian visual chromatic
and achromatic contrast between plain and carotenoid-
enriched seeds did not differ significantly from the amount
of contrast within each seed type (Table 1). We are con-
fident that the unnatural light environment used in this
experiment did not affect bird behavior, as they ate the
same amount of seed (2–3 g) as did birds in a similar
experiment with non-filtered light (Bascun
˜a
´n et al. 2009).
For the food choice tests, we measured out 10 g of each
seed type into separate white dishes and presented them
simultaneously to each bird for 1 h (Bascun
˜a
´n et al. 2009).
The dishes were 15 cm apart, and we randomized the
spatial presentation of the carotenoid-enriched and control
food. We carried out two feeding tests per bird on separate
days (11 and 13 November 2010), beginning at 0700 hours
and following an overnight period of food deprivation. At
the conclusion of each test, we quantified food consump-
tion by measuring the mass of the food remaining in each
dish. We did not take into account the spilled seeds because
the number of seed on the floor of the cage were negligible
compared to the amount of seed eaten by the birds.
Table 1 Avian visual model contrast values within a seed type and between plain and carotenoid-enriched seeds under experimental lighting
conditions
Contrast within (jnds) Contrast between (jnds) tdfp
Chromatic plain 2.33 ±0.20 2.54 ±0.12 -0.95 328 0.34
Chromatic carotenoid 2.34 ±0.13 -0.93 328 0.35
Achromatic plain 11.78 ±0.88 12.58 ±0.62 -0.74 328 0.46
Achromatic carotenoid 12.52 ±0.83 -0.059 328 0.95
J Ornithol (2012) 153:1017–1023 1019
123

Odor discrimination test
To test whether or not finches prefer to feed on foods
scented with a carotenoid-derived aroma, we presented two
dishes of the plain seed, as described above, and affixed a
5-cm
2
piece of b-ionone-scented or sham-scented filter
paper above the dishes. We did not scent the food directly
with b-ionone because we did not want to change the food
taste. The b-ionone scent consisted of a mixture of 20 ll
b-ionone (96% I12603; Sigma-Aldrich, St. Louis, MO, USA)
in 980 ll sunflower oil applied to the filter paper. This
mixture yields a b-ionone concentration of 1.89 lgg
-1
seed,
which is consistent with the concentrations found in ripe
fruits (Beekwilder et al. 2008). The sham stimulus was
simply 1 ml plain sunflower oil applied to the filter paper.
We carried out a single test per bird on 22 November 2010,
following the same procedure as the carotenoid discrimina-
tion test above.
Statistics
All statistical analyses were carried out with SPSS 13.0
(SPSS, Chicago, IL, USA) with aset at 0.05. To test for
food preferences, we used repeated-measures analyses of
variance (rmANOVA), with seed type or odor treatment as
the within-subjects factor and capture location as the
between-subjects factor. In the comparison of carotenoid-
enriched and control foods, one of the samples from a Site 3
bird was lost (spilled), resulting in a final sample sizes of 15
from Site 1, 15 from Site 2, and 14 from Site 3. Plumage
color was not included as a factor in the rmANOVA
because finches trapped at the three sites have significantly
different colors (unpublished data) and color measures were
only available for a subset of the males: 12 from Site 1, 12
from Site 2, and 13 from Site 3. Instead, we ran correlations
between the proportion of carotenoid-enriched seeds eaten
and plumage hue for the three sites. We tested the statistical
power of our tests using the pwr package (Champely 2009)
in R 2.10 (R Development Core Team 2010) and the effect
sizes reported by Senar et al. (2010).
Results
Finches did not consume significantly different amounts of
plain versus carotenoid-enriched seeds in the first experi-
ment (F
1,40
=0.725, p=0.40; Fig. 1a), nor did they con-
sume significantly different amounts of seed from the
b-ionone-scented versus control dishes (F
1,41
=1.22, p=
0.28; Fig. 1b). There was no significant effect of capture
location on food preference (carotenoid discrimination test:
F
2,40
=2.29, p=0.12; odor discrimination test: F
2,41
=
1.6, p=0.21) or the total amount of food eaten (carotenoid
discrimination test: F
2,41
\1.31, p=0.28; odor discrimi-
nation test: F
1,40
=2.29, p=0.12) during either experi-
ment. Finally, we did not find any significant regressions
between plumage coloration and food preference during the
carotenoid discrimination test (Site 1: F
1,11
=0.63, p=
0.45; Site 2: F
1,11
=0.002, p=0.96; Site 3: F
1,12
=1.9,
p=0.19) and the odor discrimination test (Site 1:
F
1,11
=0.74, p=0.41; Site 2: F
1,11
=0.008, p=0.98;
Site 3: F
1,12
=0.26, p=0.62).
With our sample size (n=45), we had sufficient power
(0.973) to detect the magnitude of carotenoid preferences
Fig. 1 a Mean ±SE mass of plain and carotenoid-enriched seeds
eaten by House Finches (Carpodacus mexicanus). bMean ±SE
mass of plain and b-ionone-scented seeds eaten
1020 J Ornithol (2012) 153:1017–1023
123

similar to those reported by Senar et al. (2010) (i.e.,
approx. 40% difference in food intake between treatments).
Discussion
To consume foods that meet nutritional and physiological
requirements, animals may employ foraging preferences for
specific nutrients using different cues like food color, taste,
or smell. For example, in food choice experiments, European
Blackcaps (Sylvia atricapilla) selected food containing
anthocyanins (antioxidant compounds) over food without
anthocyanins (Schaefer et al. 2008). Recently, Senar et al.
(2010) observed that Great Tits discriminate between
carotenoid-rich and -poor foods that were visually indistin-
guishable, and suggested that they may use non-visual cues
such as taste or smell to assess carotenoid content.
Avian olfaction has been seldom considered in behav-
ioral ecology research (i.e., mostly in navigational studies;
Wallraff 2004), and very few studies have examined how
birds use smell in the context of foraging (Nevitt et al.
1995; Roth et al. 2008; Kelly and Marples, 2004). This is
especially the case in passerines, for which olfactory bulb
size is very small compared to other species (Bang and
Cobb 1968). Previously, a study on Blue Tits (Cyanistes
caeruleus) showed that birds are more attracted to feeder
boxes with lavender odor than odorless feeder boxes, after
a period during which birds were trained to associate lav-
ender odor with food (Mennerat et al. 2005). Another study
found an additive effect of novel color and novel odor on
food consumption in Zebra Finches (Taeniopygia guttata;
Kelly and Marples 2004). However, in the same study,
birds did not react to the novel odor alone.
In our study, we tested the possibility that House Fin-
ches detect carotenoids in their food using smell. We did
not find evidence for non-visual carotenoid discrimination.
These negative results obtained are unlikely to have
resulted from experimental limitations for several reasons.
First, we used a greater difference in carotenoid concen-
tration between carotenoid-enriched and plain seed than
did Senar et al. (2010). Second, we used a larger sample
size (n=45), giving us ample power to detect the effects
reported in previous food-choice experiments with birds
(Senar et al. 2010; Schaefer et al. 2008). Finally, our
manipulation of food color and lighting conditions ensured
that visual cues could not influence food preference.
Several hypotheses could explain the absence of food
preference in our experiments. First, natural sources of
carotenoids potentially contain flavors and odorants not
present in our experimental manipulations. Many of the
flavors and aromas of fruits are generated through the
specific enzymatic cleavage of carotenoids during ripening
(Britton 2008), and may have been absent in the purified
carotenoid supplement we used in our study. In addition,
b-ionone is one of the numerous carotenoid-derived aromas
(b-damascenone; for example, Winterhalter and Rouseff
2002; Beekwilder et al. 2008), but it is possible that other
specific aromas or flavors could be used by birds to dis-
criminate carotenoid content. Second, it remains possible
that House Finches use non-visual cues to find carotenoids
in the diet at other times of the year, especially during molt
when House Finches are most likely to be avid carotenoid-
seekers to develop carotenoid-based coloration (Hill et al.
2002). Third, a species’ foraging ecology may affect the
likelihood and strength of carotenoid detection in food as
well as what detection cues are used. For example, House
Finches eat primarily seeds and fruits (Hill 1993), which
often use color to attract birds (Willson and Whelan 1990).
Thus, finches may rely heavily on these visual cues to
locate and discriminate food. For example, House Finches
have distinct food color preferences, with an aversion to
yellow and a preference for red and green (Bascun
˜a
´n et al.
2009; Stockton-Shields 1997). In contrast, tits primarily eat
insects that tend to be camouflaged or display aposematic
coloration with chemical defenses (Royama 1970), such
that coloration may not be a reliable indicator of food
quality, and non-visual cues like taste and smell may be
used instead.
In our experiments, plumage color did not influence
food preference during the carotenoid and odor discrimi-
nation tests. Previously, Bascun
˜a
´n et al. (2009) found that
redder birds demonstrated a higher degree of food selec-
tivity, measured as the proportion of their preferred food
color consumed. Thus, it is possible that redder birds may
be more selective, using non-visual cues, on the specific
food with the amount of carotenoids physiologically nee-
ded, but our study does not rule out this hypothesis. Future
experiments may examine this question by giving repeat-
edly different foods (with the same color) with several
levels of carotenoids and assessing the potential link
between food selectivity and coloration.
Birds may also develop preferences for carotenoid-rich
food sources through post-ingestive feedback mechanisms
(Yearsley et al. 2006). Carotenoids may provide a positive
feedback through their antioxidant and immune-enhancing
effects (McGraw 2006), and studies of other bird species
demonstrate the conditioned discrimination of certain
nutrients and by-products through negative or positive post-
ingestive feedback (Clark and Mason 1987; Werner et al.
2008). Our study does not rule out this possibility because
birds had access to carotenoid-enriched food only two times
during 1 h. If such learning is an important part of carot-
enoid foraging, it will be particularly interesting to examine
which cues (e.g., color, aroma, flavor) are the most salient
because such foraging preferences may influence mate
choice and shape sexual selection. For example, the
J Ornithol (2012) 153:1017–1023 1021
123

evolution of carotenoid-based sexually selected coloration
in guppies (Poecilia reticulata) and sticklebacks (Gaster-
osteus aculeatus) has been linked to foraging preferences
for carotenoid-rich foods (Rodd 2002; Smith et al. 2004).
This linkage has typically been discussed as a heritable bias
for particular traits; however, recently, learned biases have
been recognized as important selective forces, with a unique
influence on the evolution of sexual signals (Cate and Rowe
2007). Thus, learning the cues associated with specific
nutrients, like carotenoids, has the potential to influence the
direction and intensity of sexual selection (e.g., Rodd 2002).
Acknowledgments This work was funded by grants from the
National Science Foundation (IOS-0910357 to K.J.M. and 0923694 to
M.B.T. and K.J.M.) and from the Fyssen Foundation to M.G. We
thank DSM Inc., Heerlen, Netherlands, for donating the carotenoid
supplement.
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