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Carotenoid coloration predicts escape performance in the House Finch
(Haemorhous mexicanus)
Author(s): Fernando Mateos-Gonzalez , Geoffrey Hill , and Wendy Hood
Source: The Auk, 131(3):275-281. 2014.
Published By: The American Ornithologists' Union
DOI: http://dx.doi.org/10.1642/AUK-13-207.1
URL: http://www.bioone.org/doi/full/10.1642/AUK-13-207.1
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Volume 131, 2014, pp. 275–281
DOI: 10.1642/AUK-13-207.1
RESEARCH ARTICLE
Carotenoid coloration predicts escape performance in the House Finch
(Haemorhous mexicanus)
Fernando Mateos-Gonzalez,
1,a
* Geoffrey Hill,
2
and Wendy Hood
2
1
Behavioral & Evolutionary Ecology Research Unit (CSIC), Natural History Museum of Barcelona, Barcelona, Spain
2
Department of Biological Sciences, Auburn University, Auburn, Alabama, USA
a
Current address: Department of Animal Ecology, Uppsala University, Uppsala, Sweden
* Corresponding author: fernandomateos@gmail.com
Received January 15, 2014; Accepted February 14, 2014; Published April 16, 2014
ABSTRACT
Carotenoid coloration has been repeatedly shown to serve as a sexually selected signal of individual quality. Across
different species, individuals showing brighter carotenoid-based signals have been found to have superior foraging
abilities, to recover faster from diseases and, in general, to enjoy a better body condition. Experiments with birds have
also shown that carotenoid supplementation can enhance flight performance, allowing birds to take off faster from the
ground. Healthy, agile individuals should be better prepared to avoid predators, so it could be expected that
individuals displaying brighter carotenoid-based coloration would show a higher escape ability from predator attacks.
To test this prediction, we measured the escape ability of male House Finches (Haemorhous mexicanus) from a human
with a net in a large aviary and related the escape ability of each individual to its breast coloration. Males with redder
feathers showed a higher individual ability to escape than duller individuals. The superior flight performance of redder
birds would be an important asset in escape from predators, as well as when foraging or maintaining a territory. In the
specific case of the House Finch, the higher escape ability of redder individuals could be the reason for their higher
overwinter survival rate.
Keywords: Haemorhous mexicanus, condition, aerobic capacity, sexual selection, predation, escape ability
La coloraci ´
on basada en carotenoides determina la capacidad de escape en el Haemorhous mexicanus
RESUMEN
Se ha demostrado que las coloraciones basadas en carotenoides funcionan como una se ˜
nal sexual de calidad
individual. En diversas especies, se ha visto que los individuos que muestran una coloraci ´
on basada en carotenoides
ma
´s brillante muestran mejores habilidades a la hora de forrajear, se recuperan antes de enfermedades y, en general,
disfrutan de una mejor condici ´
on f´
ısica. Tambi ´
en se ha podido constatar experimentalmente que una
suplementaci ´
on de carotenoides en la dieta produc´
ıa mejoras en el vuelo de las aves, al ser capaces ´
estas de
despegar ma
´sra
´pido del suelo. Un individuo ma
´sa
´gil y de mejor salud deber´
ıa estar potencialmente mejor
preparado para escapar de predadores, de modo que podr´
ıa esperarse que individuos que muestran una coloraci ´
on
basada en carotenoides ma
´s brillante deber´
ıan ser mejores escapando del ataque de un predador. Para probar esta
predicci ´
on, medimos la habilidad de escape de machos de Haemorhous mexicanus, al ser perseguidos por un
humano con una red en un aviario, y relacionamos la capacidad de escape de cada individuo con la coloraci´
on del
plumaje del pecho. Los machos de plumas ma
´s rojas mostraron una mayor capacidad individual de escape. Esta
mejor capacidad de vuelo podr´
ıa no s ´
olo ser una valiosa habilidad contra predadores, sino tambi ´
en podr´
ıa ofrecer
importantes ventajas a la hora de forrajear o mantener un territorio. En el caso espec´
ıfico del Haemorhous mexicanus,
esta mayor capacidad de escape podr´
ıa ser la causa de la mayor supervivencia invernal de los individuos de plumas
ma
´s rojas.
Palabras clave: Haemorhous mexicanus, condici ´
on, capacidad aer ´
obica, selecci ´
on sexual, depredaci ´
on, capacidad
de escape
INTRODUCTION
Locomotor performance is a key component of survival for
many species of animals. Moreover, because courtship
behavior, competition for females, or the maintenance of a
territory are often determined by locomotor performance,
sexual selection can play a role in shaping locomotor
evolution (Husak et al. 2006, Husak & Fox 2008).
Secondary sexual traits can evolve to signal whole-
organism performance abilities, and such traits can
function in male–male competition, e.g., the horn of the
beetle Euoniticellus intermediu (Vanhooydonck et al. 2005)
Q2014 American Ornithologists’ Union. ISSN 0004-8038, electronic ISSN 1938-4254
Direct all requests to reproduce journal content to the Central Ornithology Publication Office at aoucospubs@gmail.com
or the dewlap of several Anolis lizards (Lailvaux et al.
2005). Prospective females could also benefit from
assessing and selecting on ornamental traits that signal,
for instance, a higher endurance, a greater aerobic capacity,
or a better locomotor performance (Irschick et al. 2008).
For example, courtship call rate is related to endurance
during exercise in the decorated cricket Gryllodes sigillatus
(Ketola et al. 2009) and swimming performance is
associated with the blue nuptial coloration of male Pecos
pupfish Cyprinodon pecosensis (Kodric-Brown & Nicoletto
1993), with the size of the sword of male green swordtails
Xiphophorus helleri (Royle et al. 2006), and with the
carotenoid coloration of male guppies Poecilia reticulata
(Nicoletto 1991).
Carotenoid pigments are the basis of many ornamental
displays of animals (Olson and Owens 2005). These
pigments cannot be synthesized de novo by animals but
must be ingested (Brush 1978). Therefore, carotenoid
coloration depends on the quantity and/or quality of the
food (Goodwin 1986) and on the physiological ability of
individuals to process carotenoids (Olson & Owens 1998).
Consequently, carotenoid coloration has been considered
as a signal of nutritional status, foraging ability, and general
condition of the individual (Hill 1999, Hill and McGraw
2006). There is experimental evidence of positive effects of
carotenoids in many aspects of animal health (Svensson
and Wong 2011). For instance, carotenoids have been
related to cognitive function (Mateos-Gonzalez et al.
2011), disease recovery (Hill and Farmer 2005), immuno-
competence, and prevention of oxidative damage (Powers
and Deruisseau 2004, Simons et al. 2012, but see Hartley
and Kennedy 2004). According to a recent hypothesis, the
aerobic capacity of an individual could be also related to its
carotenoid coloration, given that the metabolism of
carotenoid pigments in the production of ornamental
coloration is intimately linked to cellular respiration (Hill
and Johnson 2012, Johnson and Hill 2013).
These beneficial effects of carotenoids have a joint
potential to influence important whole-animal perfor-
mance abilities such as locomotor performance. In fact,
Blount and Matheson (2006) observed that carotenoid
supplementation enhanced takeoff performance in Zebra
Finches Taeniopygia guttata. These results agreed with
previous experiments in which Birkhead et al. (1998)
observed that Zebra Finches whose carotenoid-based red
beaks were redder evaded capture better than those with
duller beaks. It could be expected that birds with brighter
carotenoid-based plumage would show better escape
abilities.
Male House Finches (Haemorhous mexicanus) have
carotenoid-based plumage that varies from pale yellow to
bright red, which they acquire after a complete prebasic
molt in the late summer/early fall (Hill 1992). This
coloration reflects the nutritional condition of its bearer
(Hill et al. 1994), and several experiments have demon-
strated that it is used as a primary criterion in female mate
choice (Hill 1990, 1991). In this study, we tested the
prediction that male House Finches showing redder
carotenoid-based breast plumage would show greater
evasion abilities. To do so, we simulated aerial predator
attacks by pursuing birds in an enclosure with a hand net.
We then related the escape ability of each individual to its
plumage coloration.
METHODS
During January 10–24, 2011, 16 male House Finches were
captured on the campus of Auburn University, Auburn,
Alabama, USA, in traps baited with seed. The hue of breast
feathers was assessed by visually comparing feather color
to plates in Kornerup and Wanscher (1983), which is a
repeatable method of determining feather hue (Hill 1998).
Feather hue is correlated to carotenoid availability in this
and many other species (Hill et al. 1994, Simons et al.
2012). Birds were measured for wing, tail, and tarsus
length, given a metal leg band with a unique number, and
transported 2 km to an outdoor aviary (3 m wide 32.5 m
high 33.8 m long). Birds were maintained on a diet of
mixed seeds and water. Experiments started in June 2011.
House Finches are highly social birds that form flocks
outside the breeding season (Hill 1993). In previous studies
(Moreno-Rueda 2003, De Neve et al. 2010), the escape
ability of birds was examined by observing the rank order
in which birds of a captive flock are captured by a
researcher. This method takes into account the flocking
behavior that has evolved in many bird species in response
to predation pressures, a behavior that can reduce the
chances of predation by increasing confusion and dilution
effects (Hamilton 1971, Cresswell 1994). However, flock
dynamics and accidental interference among birds can
mask individual abilities. To determine the escape perfor-
mance of our experimental birds, we obtained two kinds of
measurements: capture rank order from an experimental
flock of 16 male House Finches and individual capture
time in isolation of these same birds.
Capture rank order was estimated by placing all birds in
a common enclosure (3 m wide 32.5 m high 33.8 m
long). Following the protocol described in De Neve et al.
(2010), FMG entered the room with a 30-cm–diameter
butterfly net and positioned himself in the middle of the
enclosure. Birds immediately reacted to this action as they
would in front of a real predator: flying away as far as
possible from the threat. As space and perches were
limited, some birds would end up being in more exposed
spots, at the edges of the flock. In that moment, the
experimenter attempted to capture one bird from the
flock, aiming for the closest or easiest individual. To
capture each bird, FMG tried to position the net over the
The Auk: Ornithological Advances 131:275–281, Q2014 American Ornithologists’ Union
276 Coloration and escape performance F. Mateos-Gonzalez, G. Hill, and W. Hood
individual when it was perched. If that individual managed
to evade the net, the experimenter would not continue
chasing the same individual, and would pursue instead
another bird within reach, doing so until a bird was
captured. Flight initiation distance (FID), that is the
distance at which an animal takes off from a potential
predator, is used as a proxy for boldness (Blumstein 2006,
Rodr´
ıguez-Prieto et al. 2011, Seltmann et al. 2012), so
individual differences in fear/boldness could potentially
determine the distance at which a bird is perched from the
predator in this setup. However, given the length of the
enclosure (3.8 m), the experimenter was at all times at a
closer distance than usual FIDs for House Finches (e.g.,
figure 2 in Valcarcel and Ferna
´ndez-Juricic 2009); this
factor created constant movement and escape interferenc-
es among birds, which makes very unlikely that boldness
could have an effect on which birds were closer to the
experimenter at any given time.
Upon capture, each bird was confined in a transport
cage within the enclosure and its band number and
capture order were noted. Using this procedure, FMG
captured 6 individuals in a row and relocated them in
individual enclosures (1.5 m wide 32.5 m high 33.8 m
long). After a 60-min rest, he performed another capture
shift in the common enclosure, capturing 6 more
individuals from the main flock, relocating them in
individual enclosures. The last 4 birds of the flock were
captured in a third capture shift after 90 min, a slightly
longer rest to compensate for the fact that they had already
been chased twice before. Each capture shift lasted no
more than 25 min.
To estimate individual capture time, tests were run in
the individual enclosures. FMG entered each individual
enclosure, positioned himself in the middle, and proceeded
to capture each individual with the same sweep net from
the previous test. In the same manner, the experimenter
tried to position the net over the bird as soon as it perched.
Capture, in every case, took place when the perched bird
failed to take off before the sweep net was over it. FMG
had already ample experience in the use of a sweep net, so
his capture performance was not likely to improve or
decrease over the course of the experiment. Despite being
less realistic than a setup with a real predator, this method
avoided ethical problems and provided more control over
the ‘‘predator’’ motivation. The effort needed to capture a
bird in a small enclosure is almost negligible, so it was
possible to chase the bird without pause, from the start of
the attempt until the bird was finally captured. This
approach ensured a relatively standardized effort, which
helped to control involuntary biases. Total capturing time
for each individual was measured using a stopwatch, and
ranged from 22 s to 290 s. After each capture, birds were
relocated to a common enclosure. No bird was injured as a
result of the experiment.
Analysis
We used an information-theoretic approach following
Grueber et al. (2011). Two global models, including all
measured variables, were defined to generate model sets
for each of the two experiments. Both the relationship
between capture rank order and color score, and the
relationship between individual capture time (log-trans-
formed to meet normality) and color score were fitted in
two multiple regressions (glm in R, family ¼gaussian).
There was no significant correlation between tarsus, wing,
and tail lengths (Pearson’s product-moment correlation;
wing–tail: P.05, r¼0.17; wing–tarsus: P.0.1, r¼0.38;
tail–tarsus: P.0.5, r¼0.16), so they were included as
covariates in both global models as they might affect
takeoff and flight ability. Diagnostic plots were inspected to
ensure normality of residuals in both models.
We standardized the input variables of these two global
models using the standardize function in the arm package
in R (Gelman et al. 2013). This package includes tools for
data analysis using regression and multilevel/hierarchical
models. The standardize function standardizes regression
predictors by centering and dividing by 2 SD.
Then we generated model sets for each analysis,
including null models, using the function dredge in the
MuMIn package (Barto´
n and Barto´
n 2013). From the full
model sets we selected ‘‘top model sets’’ using a 95%
confidence threshold. Finally, we computed the model-
averaged parameters, using the function model.avg in
MuMIn package (Barto´
n and Barto´
n 2013). All statistical
analyses were conducted in R 3.0.0 (R Development Core
Team 2013).
RESULTS
Capture rank order and individual capture time in
isolation were moderately correlated measures (Pearson’s
product-moment correlation: n¼16, r¼0.53, P¼0.034;
Spearman’s rank correlation: n¼16, r
s
¼0.49, P¼0.055).
An ANCOVA, with experiment (individual capture time or
capture order) as grouping factor, color score as dependent
variable, and standardized time/order as independent
variable, showed that the interaction between experiment
and color score was not significant (P,0.5). This result
indicates that the standardized slopes of color score on
capture rank order (b¼0.357 6SE ¼0.32) and color score
on individual capture time (b¼0.674 6SE ¼0.286) did
not differ significantly.
There was no significant effect of coloration, tarsus
length, wing length, or tail length in the capture order of
male House Finches (Table 1). The highest-ranking model
could not be distinguished from the null model, given that
the difference in corrected Akaike Information Criterion
(AIC
c
) was less than 2. The model-averaged parameter
estimate for all the variables overlapped zero (Table 2), so
The Auk: Ornithological Advances 131:275–281, Q2014 American Ornithologists’ Union
F. Mateos-Gonzalez, G. Hill, and W. Hood Coloration and escape performance 277
there is little evidence that any of these explanatory
variables affected capture order.
However, birds with higher color scores took longer to
capture in the individual enclosures than birds with duller
colors (Figure 1). The highest-ranking model (Table 3)
included only color score. The difference in AIC
c
between
the best model and the alternative models was larger than
2, indicating that they can be discriminated. The model-
averaged parameter estimate for color score did not
overlap zero (Table 4), indicating a significant effect of
this variable on capture time.
DISCUSSION
As predicted by the hypothesis that red carotenoid
coloration is a condition-dependent signal of individual
quality (Hill 1990), we observed that male House Finches
with redder plumage coloration were harder to capture
with a sweep net than birds with duller colors.
In contrast to the significant relationship between
individual escape performance and coloration, we found
no significant relationship between capture rank and
feather color, despite both measures being moderately
correlated. We speculate that the lack of relationship
between rank order of capture of House Finches and their
feather color stems from the interference among flock
members that obscures individual ability. When 16 House
Finches are being chased in a cage, they frequently crowd
onto perches and into corners. The vision and movements
of some birds are impaired. When a single bird is chased in
a cage following our protocol, in contrast, probably the
ability to continue to fly is what determines capture time.
Hence, individual capture time is a measure that will better
reproduce individual performance, which is in turn
reflected by the sexual carotenoid-based signal.
In our trials, all birds were captured when they were
perched and failed to take off before the experimenter
attempted to put a sweep net over them. Thus, birds that
TABLE 1. Top models for capture order, resulted from the model
average after selection of a 95% confidence model set. Models
in the set are arranged from best to worst based on the
difference in AIC
c
values between the best model and
competing models (DAIC
c
). AIC weights (AIC
w
) are the relative
likelihoods of a model given the data, and evidence ratios (ER)
are the relative likelihood of each model versus the best model.
Models AIC
c
DAIC
c
AIC
w
ER
Tail length 98.75 0 0.31 1
Null model 99.23 0.48 0.24 1.29
Color score 100.95 2.19 0.10 3.1
Tail L þWing L 101.23 2.48 0.09 3.44
Color score þTail L 101.82 3.07 0.07 4.43
Wing length 101.91 3.15 0.06 5.17
Tarsus length 102.22 3.46 0.05 6.2
Tail length 102.39 3.64 0.05 6.2
Color score þTarsus L 103.35 4.60 0.03 10.33
TABLE 2. Standardized coefficients of model predictors, after
model averaging of the top candidate models (95% confidence)
(see Table 1). Table includes estimates, relative importance (R,
sum of Akaike weights of the models in which the predictor was
present), unconditional SE, and 95% confidence interval (CI) for
estimates. Parameter estimates have a significant effect when
the 95% CIs do not include zero.
Predictors PEstimate SE 2.5% 97.5%
Tail length 0.51 4.256 2.325 9.255 0.742
Color score 0.2 2.599 2.637 3.028 8.227
Wing length 0.15 1.958 2.430 3.263 7.178
Tarsus length 0.13 0.970 2.782 6.883 4.944
FIGURE 1. Relationship between color score of the different
individuals and time required to capture each one (log
transformed). The line represents the regression slope.
TABLE 3. Top models for individual capture time, resulting from
the model average after selection of a 95% confidence model
set. Models in the set are arranged from best to worst based on
the difference in AIC
c
values between the best model and
competing models (DAIC
c
). AIC weights (AIC
w
) are the relative
likelihoods of a model given the data, and evidence ratios (ER)
are the relative likelihood of each model versus the best model.
Models AIC
c
DAIC
c
AIC
w
ER
Color score 35.9 0 0.44 1
Null model 38.2 2.23 0.14 3.14
Color score þTarsus L 38.7 2.72 0.11 4
Color score þTail L 39.1 3.21 0.09 4.89
Color score þWing L 39.4 3.44 0.08 5.5
Tail length 39.9 3.99 0.06 7.33
Tarsus length 41.1 5.14 0.03 14.67
Wing length 41.2 5.26 0.03 14.67
Color score þTail L þTarsus L 42.9 6.97 0.01 44
The Auk: Ornithological Advances 131:275–281, Q2014 American Ornithologists’ Union
278 Coloration and escape performance F. Mateos-Gonzalez, G. Hill, and W. Hood
managed to take off faster and perched for shorter periods
were probably better able to evade capture, which could
indicate that these birds had a greater aerobic capacity
than males with less-red plumage. A recent hypothesis
proposes that carotenoid coloration links to performance
because the metabolism of carotenoid pigments in the
production of ornamental coloration is intimately linked to
cellular respiration (Hill and Johnson 2012, Johnson and
Hill 2013). Our results could suggest that the potential
greater aerobic capacity of redder birds is derived from a
more efficient cellular respiration (Hill and Johnson 2012,
Johnson and Hill 2013).
Carotenoid coloration has also been hypothesized to
reflect other aspects of condition beside cellular respira-
tion including energy stores, reduced oxidative stress, and
enhanced immunocompetence (Svensson and Wong 2011,
Simons et al. 2012). Any one of these aspects of condition
could explain the relationship between carotenoid color-
ation and capture evasion. Carotenoids could also have a
direct effect on flight performance. Blount and Matheson
(2006) reported that birds that had been supplemented
with carotenoids improved their takeoff capability, a skill
that seemed to be of importance in our experiments. Even
though our birds were maintained with the same diet,
individual variation in absorption or allocation of pigments
could result in some individuals having access to more
circulating carotenoids. These individuals could then take
advantage of the potential beneficial effects of carotenoids,
such as reduced oxidative muscle damage, enhanced
motor performance or cognition processes, and improved
immune defense (Blount and Matheson 2006, Svensson
and Wong 2011, Simons et al. 2012).
In addition to simply allowing them to avoid being
captured and killed, the greater escape ability of redder
male House Finches could confer on them important
fitness advantages when defending their nest against
predators (Reyer et al. 1998). Better flight ability could
also enable more efficient foraging, which could in turn
result in better parental care. This advantage would grant
direct benefits to female House Finches choosing redder
males (Hill 1990).
Female House Finches are dominant over males
(Thompson 1960) and more aggressive toward drabber
males (Belthoff and Gowaty 1996). This higher aggression
could be a reason for drabber males to change social
groups more frequently than the more stable redder males
(Oh and Badyaev 2010). The stability of redder males in
social groups could be driven by a social female preference
for males with higher foraging and antipredator abilities.
Ultimately, the lower female aggression toward redder
males, and their more efficient foraging and better
antipredator abilities, could jointly explain the higher
overwinter survival rate of redder House Finches (Hill
1991, Belthoff and Gowaty 1996).
ACKNOWLEDGMENTS
We thank A. J. Pate for his help during the experiments and
Andrew Arnold and Meagan Duval for help capturing birds.
We thank Mirjam Amcoff, Bj¨
orn Rogell, and G¨
oran Arnqvist
for statistical advice. Mirjam Amcoff, Fredrik Sundstr¨
om,
Gregorio Moreno-Rueda, Keith Tarvin, and two anonymous
reviewers made helpful comments on the manuscript. This
work was funded by NSF grant IOS0923600 to G. E. H. and F.
P. I., and BES-2007-16320 grant to F. M. G. (Spanish Ministry
of Science and Technology). Birds were maintained under
USFWS migratory bird permit MB784373-2 and Alabama
State permit 2010000072968680 and IACUC project 2011-
1939. The authors declare no conflict of interest.
LITERATURE CITED
Barto ´
n, K., and M. K. Barto ´
n (2013). Package ‘MuMIn’: Model
selection and model averaging based on information criteria.
R package version 1.9.13.
Belthoff, J. R., and P. A. Gowaty (1996). Male plumage coloration
affects dominance and aggression in female house finches.
Bird Behavior 11:1–7.
Birkhead, T. R., F. Fletcher, and E. J. Pellatt (1998). Sexual
selection in the Zebra Finch Taeniopygia guttata: Condition,
sex traits and immune capacity. Behavioral Ecology and
Sociobiology 44:179–191.
Blount, J. D., and S. M. Matheson (2006). Effects of carotenoid
supply on escape flight responses in zebra finches, Taenio-
pygia guttata. Animal Behaviour 72:595–601.
Blumstein, D. T. (2006). Developing an evolutionary ecology of
fear: How life history and natural history traits affect
disturbance tolerance in birds. Animal Behaviour 71:389–399.
Brush, A. H. (1978). Avian pigmentation. In Chemical Zoology (A.
Brush, Editor). Aves, Vol. 10:141–161. Academic Press, New
York, NY, USA.
Cresswell, W. (1994). Flocking is an effective anti-predation
strategy in redshanks, Tringa totanus. Animal Behaviour 47:
433–442.
De Neve, L., J. D. Iba
´˜
nez- ´
Alamo, and M. Soler (2010). Age- and
sex-related morphological and physiological differences
TABLE 4. Standardized coefficients of model predictors, after
model averaging of the top candidate models (95% confidence)
(see Table 3). Table includes estimates, relative importance (R,
sum of Akaike weights of the models in which the predictor was
present), unconditional SE, and 95% confidence interval (CI) for
estimates. Parameter estimates have a significant effect when
the 95% CIs do not include zero (highlighted in bold).
Predictors PEstimate SE 2.5% 97.5%
Color score 0.73 0.776 0.343 0.039 1.513
Tarsus length 0.16 0.227 0.426 1.131 0.677
Tail length 0.16 0.266 0.367 1.052 0.519
Wing length 0.11 0.074 0.366 0.858 0.711
The Auk: Ornithological Advances 131:275–281, Q2014 American Ornithologists’ Union
F. Mateos-Gonzalez, G. Hill, and W. Hood Coloration and escape performance 279
influence escape capacity in House Sparrows (Passer domes-
ticus). Canadian Journal of Zoology 88:1021–1031.
Gelman, A., Y. S. Su, M. Yajima, M. Y. S. Su, and I. Matrix (2013).
Package ‘arm’: Data analysis using regression and multilevel/
hierarchical models. R package version 1.6–10.
Goodwin, T. W. (1986). Metabolism, nutrition, and function of
carotenoids. Annual Review of Nutrition 6:273–297.
Grueber, C. E., S. Nakagawa, R. J. Laws, and I. G. Jamieson (2011).
Multimodel inference in ecology and evolution: Challenges
and solutions. Journal of Evolutionary Biology 24:699–711.
Hamilton, W. D. (1971). Geometry for the selfish herd. Journal of
Theoretical Biology 31:295–311.
Hartley, R. C., and M. W. Kennedy (2004). Are carotenoids a red
herring in sexual display? Trends in Ecology & Evolution 19:
353–354.
Hill, G. E. (1990). Female house finches prefer colourful males:
Sexual selection for a condition-dependent trait. Animal
Behaviour 40:563–572.
Hill, G. E. (1991). Plumage coloration is a sexually selected
indicator of male quality. Nature 350:337–339.
Hill, G. E. (1992). Proximate basis of variation in carotenoid
pigmentation in male House Finches. The Auk 109:1–12.
Hill, G. E. (1993). House Finch (Carpodacus mexicanus). In The
Birds of North America, no. 46 (A. Poole, Editor). The Birds of
North America Online, Ithaca, New York, USA.
Hill, G. E. (1998). An easy, inexpensive method to quantify
plumage coloration. Journal of Field Ornithology 69:353–363.
Hill, G. E. (1999). Mate choice, male quality, and carotenoid-
based plumage coloration. In Proceedings of the 22nd
International Ornithology Congress (N. J. Adams and R. H.
Slotow, Editors). BirdLife South Africa, Johannesburg, South
Africa. pp. 1654–1668.
Hill, G. E., and K. L. Farmer (2005). Carotenoid-based plumage
coloration predicts resistance to a novel parasite in the house
finch. Naturwissenschaften 92:30–34.
Hill, G. E., and J. D. Johnson (2012). The vitamin A–redox
hypothesis: A biochemical basis for honest signaling via
carotenoid pigmentation. The American Naturalist 180:E127–
E150.
Hill, G. E., and K. J. McGraw (2006). Bird Coloration. Volume 2:
Function and Evolution. Harvard University Press, Cambridge,
MA, USA.
Hill, G. E., R. Montgomerie, C. Y. Inouye, and J. Dale (1994).
Influence of dietary carotenoids on plasma and plumage
colour in the house finch: Intra- and intersexual variation.
Functional Ecology 8:343–350.
Husak, J. F., and S. F. Fox (2008). Sexual selection on locomotor
performance. Evolutionary Ecology Research 10:213–228.
Husak, J. F., F. F. Stanley, M. B. Lovern, and R. A. Bussche (2006).
Faster lizards sire more offspring: Sexual selection on whole-
animal performance. Evolution 60:2122–2130.
Irschick, D. J., J. J. Meyers, J. F. Husak, and J. Le Galliard (2008).
How does selection operate on whole-organism functional
performance capacities? A review and synthesis. Evolutionary
Ecology Research 10:177–196.
Johnson, J. D., and G. E. Hill (2013). Is carotenoid ornamentation
linked to the inner mitochondria membrane potential? A
hypothesis for the maintenance of signal honesty. Biochimie
95:436–444.
Ketola, T., R. Kortet, and J. S. Kotiaho (2009). Endurance in
exercise is associated with courtship call rate in decorated
crickets, Gryllodes sigillatus. Evolutionary Ecology Research
11:1131–1139.
Kodric-Brown, A., and P. F. Nicoletto (1993). The relationship
between physical condition and social status in pupfish
Cyprinodon pecosensis. Animal Behaviour 46:1234–1236.
Kornerup, A., and J. H. Wanscher (1983). Methuen Handbook of
Colour. Methuen, London, England.
Lailvaux, S. P., J. Hathway, J. Pomfret, and R. J. Knell (2005). Horn
size predicts physical performance in the beetle Euoniticellus
intermedius (Coleoptera: Scarabaeidae). Functional Ecology
19:632–639.
Mateos-Gonzalez, F., J. Quesada, and J. C. Senar (2011). Sexy
birds are superior at solving a foraging problem. Biology
Letters 7:668–669.
Moreno-Rueda, G. (2003). The capacity to escape from predators
in Passer domesticus: An experimental study. Journal f¨
ur
Ornithologie 144:438–444.
Nicoletto, P. F. (1991). The relationship between male ornamen-
tation and swimming performance in the guppy, Poecilia
reticulata. Behavioral Ecology and Sociobiology 28:365–370.
Oh, K. P., and A. V. Badyaev (2010). Structure of social networks
in a passerine bird: Consequences for sexual selection and
the evolution of mating strategies. The American Naturalist
176:E80–E89.
Olson, V. A., and I. P. F. Owens (1998). Costly sexual signals: Are
carotenoids rare, risky or required? Trends in Ecology &
Evolution 13:510–514.
Olson, V. A., and I. P. F. Owens (2005). Interspecific variation in
the use of carotenoid-based coloration in birds: Diet, life
history and phylogeny. Journal Evolutionary Biology 18:
1534–1546.
Powers, S. K., K. C. Deruisseau, J. Quindry, and K. L. Hamilton
(2004). Dietary antioxidants and exercise. Journal of Sports
Sciences 22:81–94.
R Development Core Team (2013). R: A Language and
Environment for Statistical Computing. R Foundation for
Statistical Computing, Vienna, Austria. http://www.R-project.
org/
Reyer, H. U., W. Fischer, P. Steck, T. Nabulon, and P. Kessler
(1998). Sex-specific nest defense in house sparrows (Passer
domesticus) varies with badge size of males. Behavioral
Ecology and Sociobiology 42:93–99.
Rodr´
ıguez-Prieto, I., J. Mart´
ın, and E. Ferna
´ndez-Juricic (2011).
Individual variation in behavioural plasticity: Direct and
indirect effects of boldness, exploration and sociability on
habituation to predators in lizards. Proceedings of the Royal
Society B: Biological Sciences 278:266–273.
Royle, N. J., N. B. Metcalfe, and J. Lindstr ¨
om (2006). Sexual
selection, growth compensation and fast-start swimming
performance in Green Swordtails, Xiphophorus helleri. Func-
tional Ecology 20:662–669.
Seltmann, M. W., M. ¨
Ost, K. Jaatinen, S. Atkinson, K. Mashburn,
and T. Hollm´
en (2012). Stress responsiveness, age and body
condition interactively affect flight initiation distance in
breeding female eiders. Animal Behaviour 84:889–896.
Simons, M. J., A. A. Cohen, and S. Verhulst (2012). What does
carotenoid-dependent coloration tell? Plasma carotenoid
level signals immunocompetence and oxidative stress state
in birds—A meta-analysis. PloS ONE 7(8):e43088.
Svensson, P. A., and B. B. M. Wong (2011). Carotenoid-based
signals in behavioural ecology: A review. Behaviour 148:131–
189.
The Auk: Ornithological Advances 131:275–281, Q2014 American Ornithologists’ Union
280 Coloration and escape performance F. Mateos-Gonzalez, G. Hill, and W. Hood
Thompson, W. L. (1960). Agonistic behavior in the House Finch.
Part I: Annual cycle and display patterns. The Condor 62:245–
271.
Valcarcel, A., and E. Ferna
´ndez-Juricic (2009). Antipredator
strategies of house finches: Are urban habitats safe spots
from predators even when humans are around? Behavioral
Ecology and Sociobiology 63:673–685.
Vanhooydonck, B., A. Y. Herrel, R. van Damme, and D. J. Irschick
(2005). Does dewlap size predict male bite performance in
Jamaican Anolis lizards? Functional Ecology 19:38–42.
The Auk: Ornithological Advances 131:275–281, Q2014 American Ornithologists’ Union
F. Mateos-Gonzalez, G. Hill, and W. Hood Coloration and escape performance 281
