Behavioral Ecology Vol. 15 No. 1: 141–147
DOI: 10.1093/beheco/arg092
Asymmetry in size, shape, and color impairs
the protective value of conspicuous color
patterns
Anders Forsmana and Joakim Herrströmb
Department of Biology and Environmental Science, Kalmar University, SE-391 82 Kalmar, Sweden,
and bSyngenta Seeds AB, Box 302, SE-261 23, Landskrona, Sweden
a
The received view of protective coloration in animals is that conspicuous colors and patterns have evolved because they elicit
avoidance behavior in potential predators. In the present study, we examine the spontaneous response of naive predators (Gallus
gallus domesticus) to artificial prey to test the hypothesis that deviations from bilateral symmetry of signaling pattern elements may
negatively influence the avoidance-inducing effect of conspicuous color patterns. Chicks displayed stronger aversions to artificial
‘‘butterfly’’ prey items possessing symmetric color pattern elements than to those possessing asymmetric signals with pattern
elements of different color or shape. Although they attacked signals with a size asymmetry of 5% at the same rate as symmetric
signals, signals with a size asymmetry of 7.5% or more were attacked more often than were symmetric signals. These results
suggest that the protective value of conspicuous color patterns is impaired by asymmetry in color, shape, and size of color pattern
elements. Our findings also argue against the notion that animals have inherent preferences for symmetric over asymmetric
objects, and demonstrate the existence of a threshold for asymmetry detection, beyond which further increments in asymmetry
have no influence on signal efficacy. Key words: asymmetry, communication, perception, predation risk, signaling. [Behav Ecol
15:141–147 (2004)]
onspicuous and simple color patterns (often red, yellow,
or white in combination with black) are common among
animals that are distasteful, noxious, or otherwise potentially
dangerous to their predators (see Cott, 1940; Summers and
Clough, 2001; Wallace, 1867). The common view is that
conspicuousness has evolved because it constitutes a strong
visual signal that is easy for receiving predators to detect,
learn, and associate with unpalatability (Alatalo and Mappes,
1996; Endler, 1991; Gittleman and Harvey, 1980; Guilford and
Dawkins, 1991; Lindström et al., 1999; Yashi and Higashi,
1998). However, conspicuous coloration may provide protection against predators even if the prey lacks chemical or
structural defense mechanisms, because coloration may elicit
spontaneous avoidance behaviors in naive predators (see
Coppinger, 1969, 1970). It has been suggested that bilateral
asymmetry also may play a role in communication, but this has
been studied primarily within the context of mate choice
(Møller, 1993; Swaddle, 1999a). In the present study, we
examine the spontaneous response of naive chicks toward
artificial prey to test the idea (Forsman and Merilaita, 1999;
Kirkpatrick and Rosenthal, 1994; Møller and Swaddle, 1997)
that asymmetry may negatively influence the protective value
of avoidance-inducing color patterns.
Several lines of evidence suggest that deviations from
bilateral symmetry of signaling color pattern elements may
influence the protective value of prey coloration. Thus,
animals appear to be perceptually sensitive to very small
deviations from bilateral symmetry (Møller, 1993; Schwabl and
Delius, 1984; Swaddle, 1999a,b). Experiments on humans
(Attneave, 1954), pigeons (Delius and Nowak, 1982), and
honeybees (Horridge, 1996) further have shown that symmetrical patterns are easier to detect, learn, and reproduce
C
Address correspondence to A. Forsman. E-mail: anders.forsman@
hik.se.
Received 23 August 2002; revised 3 February 2003; accepted 13
March 2003.
from memory than are asymmetric ones. On the one hand,
this raises the possibility that symmetry of visual warning
signals may improve avoidance learning by predators (Forsman and Merilaita, 1999; Kirkpatrick and Rosenthal, 1994;
Møller and Swaddle, 1997). On the other, if asymmetric
signals are more difficult to perceive and elicit a weaker
neural response compared with symmetric signals (Osorio,
1996), one would expect naive predators to show stronger
unconditioned avoidance behaviors toward prey with symmetric color patterns. It has also been suggested that organisms
may exhibit inherent general preferences for symmetric over
asymmetric objects, although the empirical evidence is
inconclusive (for review, see Swaddle, 1999a). Such general
symmetry preferences would render predators more inclined
to attack prey with symmetric than with asymmetric color
patterns. To discriminate between these competing hypotheses, we conducted a series of experiments to study the effects
of signal color and asymmetry on unconditioned aversions to
conspicuously colored prey by presenting naive domestic
chickens (Gallus gallus domesticus) to pairs of artificial paper
‘‘butterflies’’ (Forsman and Merilaita, 1999). Visual stimuli
may be said to resemble ‘‘multicomponent’’ signals (Rowe,
1999) in the sense that different aspects of the stimulus are
handled separately and may differently affect the perception
of and response to the signal (Osorio et al., 1999). We
therefore performed separate tests for effects of asymmetry in
color, shape, and size of the signaling pattern elements.
Several previous studies have shown that color influences the
protective value of warning signals (see Coppinger, 1969, 1970;
Osorio et al., 1999), but few attempts have been made to
examine the role of color in symmetry perception (but see
Morales and Pashler, 1999; Zhang and Gerbino, 1992). There is
experimental evidence to suggest that the response of females
to male secondary sexual ornaments is influenced by color
asymmetry. For instance, Swaddle and Cuthill (1994) showed
that female zebra finches choose symmetrically leg-banded
males over asymmetrically banded ones. To our knowledge,
Behavioral Ecology vol. 15 no. 1 International Society for Behavioral Ecology 2004; all rights reserved.
Behavioral Ecology Vol. 15 No. 1
142
asymmetry detection that did incorporate an element of
individual learning, Swaddle (1999b) showed that European
starlings could accurately discriminate 1.8% asymmetry from
symmetry but was unable to discriminate 1.25% asymmetric
stimuli from symmetric patterns. In the present study, we test
the hypothesis that there may exist an asymmetry threshold
beyond which further increments in size asymmetry levels do
not influence the magnitude of the initial response of naive
predators to avoidance-inducing signals.
METHODS
Predators and artificial prey items
Figure 1
Artificial paper butterflies presented to chicks in the six experiments
used to test for effects on unconditioned predator aversions of color,
shape, and asymmetry in color, shape, and size of pattern elements of
conspicuously colored prey. The isolated figure at the right is an inset
showing the dimensions of the butterflies. The size and shape of the
butterflies and the position of the food crumb was identical in all
experiments and trials. The figure shows the color, shape, and size of
the signaling pattern elements of the two types of butterflies
presented simultaneously to birds in each experiment and trial, and
the number of birds used in each treatment. Numbers running along
the base of the butterflies in experiment 6 represent the diameter (in
mm) of the left and right spot. See text for details.
however, no study has tested the hypothesis that color
asymmetry may negatively influence the protective value of
warning signals.
With few exceptions (Merilaita, 1998; Summers and
Clough, 2001), animal color patterns show a high degree of
bilateral symmetry in shape of pattern elements (Wallace,
1889). This may reflect either developmental constraints or
selection against asymmetric phenotypes (Forsman and
Merilaita, 1999). In the present study, we test if the protective
value of avoidance-inducing signals is impaired by shape
asymmetry.
A central question in understanding the role of asymmetry
in the evolution of signaling is the perceptual capability of
predators to detect and discriminate symmetric from asymmetric signals (Swaddle, 1999a,b). Because the mean asymmetry in natural populations typically constitutes only 1–2%
of trait size, it has been suggested that most individuals may be
perceived as symmetric (Swaddle, 1999a). In a recent experiment designed specifically to investigate the limits to
As predators naive domestic chicks (G. gallus domesticus) were
used on days 5–7 after hatching. Before trials, birds were
housed by a commercial breeder in a 1200-m2 hangar at 30 C,
60% relative humidity, 21 h light/3 h dark photo-period,
stocking density of 17 individuals/m2, and with food and
water ad lib. The experimental arena consisted of a beige 40
3 30 3 40 cm plastic cage, the bottom of which was covered
with sawdust. Artificial paper butterflies were used as prey (see
Forsman and Merilaita, 1999). Butterflies were made from
black paper and measured 40 mm wide, 30 mm high, and 20
mm ‘‘girth’’ (Figure 1). Each butterfly was affixed under
a plastic Petri dish (diameter ¼ 55 mm). Inside the dish, one
chick-starter food crumb (approximately 3–4 mm in diameter
and beige to yellowish brown in color) was placed at the
middle of the butterfly. The food crumbs used in the
experiments were identical to those provided by the breeder
as food for the birds when maintained in the hangar. Because
the food crumb was always placed over the midbody of the
black butterfly (Figure 1), it was equally conspicuous across
the paired butterflies tested within each treatment.
At the onset of a trial, two individual birds (to avoid
stressing the birds) were transferred to the experimental cage
containing the two types of butterflies (monochromatic black
versus black with signaling colored pattern elements or
symmetric versus asymmetric) placed side by side. A trial was
terminated when one of the two birds had eaten or pecked at
the food crumb on one of the two presented butterflies, in
which case both birds were replaced to avoid confounding
effects owing to social learning (Sherwin et al., 2002).
Preliminary observations revealed that birds that had made
no attempt to peck at the food crumb within the first 60 s were
very unlikely to do so even if remaining in the experimental
cage for up to 10 min. Trials were therefore also terminated if
none of the birds had attacked the butterfly within 3 min, in
which case one of the birds was replaced. The exact duration
of trials was not recorded but ranged from 5–120 s. Each bird
was allowed to choose only once and presented only two
different butterflies. After the experiments, the birds were
returned to the hangar.
In the series of experiments described below each part was
designed in the light of the results of the previous one.
Experiment 1: testing for effects of spot color
The first experiment was designed to test if the protective
value of conspicuous coloration depends on the color of the
signaling pattern elements. Birds were offered a choice
between a monochrome black butterfly and a black butterfly
with two signaling circular spots (diameter ¼ 9.49 mm). Birds
were divided into four treatments according to spot color
(Figure 1). The spot colors used in the four treatments were
blue (Natural Colour System code B:1060), red (Y90R:1070),
yellow (Y10R:1070), and white (pure white). For each
treatment, 30 naive birds were used. We expect butterflies
Forsman and Herrström
•
Signal asymmetry and predation risk
with colored spots to suffer a lower rate of food-crumb
removal compared with monochromatic butterflies, under
the hypothesis that birds have stronger unconditioned
aversions to more conspicuous color patterns.
Experiment 2: testing for effects of spot color asymmetry
To test the hypothesis that the protective value of warning
signals is influenced by color asymmetry, a new set of birds
were presented with two butterflies simultaneously, one with
two spots of the same color and another with two spots of
different color (Figure 1). Two different treatments were
used, and 50 naive birds were used for each of the two
treatments. In the first treatment, a butterfly with two red
spots was presented together with a butterfly with one red
spot and one yellow spot. In the second treatment, a butterfly
with two white spots was presented together with a butterfly
with one white spot and one yellow spot. These particular
color combinations were chosen because the results from
experiment 1 revealed that the birds showed significant
aversions only toward yellow spots but tended to be attracted
to white spots (see below). Thus, if the avoidance-inducing
effect of yellow is stronger than the avoidance-weakening
effect of color asymmetry, one would expect birds in the first
treatment to avoid the asymmetric butterfly with one yellow
spot and instead peck first at the symmetric butterfly with two
red spots. By the same line of argument, one would expect
birds in the second treatment to peck first at the symmetric
butterfly with two white spots (to which they are attracted)
and avoid the asymmetric butterfly with one yellow spot. In
contrast, the hypothesis that avoidance-inducing signals are
impaired by color asymmetry predicts symmetric butterflies to
suffer a lower rate of food-crumb removal.
Experiment 3: testing for effects of pattern shape
This experiment was designed to test the hypothesis that
efficacy of conspicuous coloration is influenced by the shape
of the signaling pattern elements (Figure 1). Because the
results of experiment 1 suggested that birds had significant
unconditioned aversions only to black butterflies with yellow
signals, we used yellow pattern elements in this and subsequent experiments. We tested the reactions of birds
presented with two butterflies with signals consisting either
two yellow circular spots (diameter ¼ 9.49 mm) or two yellow
squares (8.41 3 8.41 mm), using 20 naive birds. To avoid
confounding effects of signaling area (Forsman and Merilaita,
1999) the area of the yellow spots and squares was identical.
Experiment 4: testing for effects of pattern shape
asymmetry
This experiment was designed to test the hypothesis that the
efficacy of conspicuous coloration is negatively influenced by
asymmetry in shape of the signaling pattern elements. For this
purpose, the reactions of birds when offered a choice between
a signal consisting of two yellow squares and a signal
consisting of one yellow square and one yellow spot were
tested, using 20 naive birds (Figure 1). This particular
combination of shapes was chosen because the results from
experiment 3 revealed that birds showed stronger aversions to
circular spots than to squares (see below). Thus, if the
stronger avoidance-inducing effect of spots compared with
squares is more important than is the avoidance-weakening
effect of shape asymmetry, one would expect birds to avoid
the asymmetric butterfly with one spot and one square and
peck first at the symmetric butterfly with two squares. In
contrast, the hypothesis that shape asymmetry impairs the
143
protective value of warning signals predicts asymmetric
butterflies to have the highest rate of food-crumb removal.
Experiment 5: testing for effects of pattern shape
asymmetry using novel signals
Although predators may be naive in the sense that they are
inexperienced, they are not naive in an evolutionary sense
(Alatalo and Mappes, 1996). To reduce the problems
associated with unlearned preferences and biases against
certain colors and patterns, we tested for effects of shape
asymmetry by using butterflies with novel pattern elements
(crosses and bars) not normally found in nature. Two
different treatments were used. In the first treatment,
a butterfly with a signal consisting of one cross and one bar
was presented together with a butterfly with a signal consisting
of two crosses (Figure 1). In the second treatment, a signal
consisting of one cross and one bar was presented with a signal
consisting of two bars. In each treatment, 40 naive birds were
used. Butterflies with one bar and one cross were expected to
have the highest rate of food-crumb removal in both
treatments, under the hypothesis that shape asymmetry
impairs the protective value of conspicuous coloration.
Experiment 6: testing for effects of pattern size asymmetry
This final experiment was designed to test the hypothesis that
the protective value of conspicuous coloration is impaired by
asymmetries in the size of pattern elements, and to test the
idea that there may exist a perceptual asymmetry threshold
beyond which further increments in asymmetry levels do not
influence the magnitude of the initial response of naive
predators to avoidance-inducing signals. For this purpose
a new set of naive birds was used. Each bird was simultaneously offered one butterfly with a symmetric signal
consisting of two equal-sized yellow spots (diameter ¼ 9.49
mm) and one butterfly with an asymmetric signal consisting
of two different-sized spots (Figure 1). Five different degrees
of size asymmetry were used, ranging from 5–33% of mean
spot size. To avoid confounding effects of signaling area
(Forsman and Merilaita, 1999), spot sizes were chosen so that
the combined area of the two yellow spots was identical in
symmetric and asymmetric signals and in all treatments. The
size (diameter, in mm) of large and small spots in the five
treatments were as follows: 5% (9.6/8.7), 7.5% (9.9/8.4), 10%
(10.0/8.2), 15% (10.5/7.7), and 33% (11.5/5.9). For each
treatment, 80 naive birds were used. We expect butterflies
with size-asymmetric signals to experience a higher overall
rate of food-crumb removal. Moreover, if the relative aversion
to symmetry is influenced by the difference in level of
asymmetry between alternative prey, one would expect the
relative rate of food-crumb removal from asymmetric butterflies to increase progressively across treatments, from the
lowest to the highest degree of spot-size asymmetry. In
contrast, the hypothesis of an asymmetry detection and
response threshold predicts the variation in relative rate of
food-crumb removal among treatments to follow a stepfunction.
RESULTS
Although the behavioral response varied among birds
presented with different kinds of butterflies, all birds seemed
intimidated and hesitated before pecking at the food crumb,
regardless of the color and shape of the signaling pattern
elements of the butterfly. Despite the large numbers of
individuals used, all birds pecked first at the food crumb and
never at the signaling pattern elements.
Behavioral Ecology Vol. 15 No. 1
144
Figure 2
The proportion of artificial black butterflies with visual warning
signals of different colors (blue, red, white, or yellow) attacked first
when presented together with a monochromatic black butterfly in
experiment 1. The dotted reference line indicates equal rate of foodcrumb removal from monochromatic and spotted butterflies. Symbols
above bars indicate results from two-tailed binomial test of a difference
from the randomly expected proportion eaten. n.s. indicates not
significant; s, .05 , p , .10; *p , .05; **p , .01.
Figure 3
Comparison of rate of food-crumb removal for color asymmetric
butterflies with two signaling spots of different color presented
together with color symmetric butterflies with a signal consisting of
two spots of the same color. Results are from experiment 2. The
symbols along the abscissa indicate the shape and color (R indicates
red; W, white; and Y, yellow) of signaling pattern elements on each of
the two prey types presented together. Symbols above bars indicate
results from two-tailed binomial tests for large samples with correction
for continuity. n.s. indicates not significant. *p , .05.
Effects of spot color
When birds were offered a choice between a monochromatic
black butterfly presented and a black butterfly with two
signaling spots, there were clear differences in the response
among birds presented with signals of different colors (v2 ¼
13.53, df ¼ 3, p ¼ .004) (Figure 2). Butterflies with blue or red
signaling spots suffered the same rate of food-crumb removal
as that of monochromatic butterflies (two-tailed binomial test
of a difference from the randomly expected proportion eaten,
that is, 50%: blue, p . .9; red, p ¼ .86), whereas butterflies
with white spots suffered a somewhat, but not significantly,
higher rate of removal than did monochromatic butterflies
without spots (p ¼ .098). Birds significantly avoided only
butterflies with two yellow spots (p ¼ .002).
Effects of color asymmetry
When birds were offered a choice between a color-symmetric
butterfly with two red spots versus an asymmetric butterfly
with one red and one yellow spot, both kinds experienced the
same rate of food-crumb removal (two-tailed binomial test for
large samples with correction for continuity, z ¼ 0.16, p ¼ .87)
(Figure 3). In contrast, butterflies with one white and one
yellow spot had a significantly higher rate of removal than did
butterflies with two white spots (z ¼ 2.12, p ¼ .034) (Figure 3).
Effects of shape and shape asymmetry
Results from experiment 3 and 4 revealed that birds
responded differently to the butterflies depending on the
shape of the signaling pattern elements, and suggest that the
protective value of conspicuous coloration is impaired by
shape asymmetry. Thus, butterflies with a signal consisting of
two circular pattern elements experienced a lower rate of
food-crumb removal than did butterflies with two squares
(two-tailed binomial test, p ¼ .012) (Figure 4A). Despite the
stronger aversion induced by circular compared with squared
pattern elements, however, shape-asymmetric butterflies with
one spot and one square had a significantly higher rate of
food-crumb removal than did symmetric butterflies with two
squares (p ¼ .002) (Figure 4A).
Effects of shape asymmetry as revealed by using
novel signals
A negative effect of shape asymmetry on the avoidanceinducing effect of the signal was also evident in the response
of birds presented butterflies with signals not normally found
in nature. Thus, butterflies with asymmetric signals consisting
of one cross and one bar suffered a higher rate of food crumb
removal compared with that of symmetric butterflies with
either two crosses (binomial test, z ¼ 2.06, p ¼ .039) or two
bars (z ¼ 2.37, p ¼ .0017) (Figure 4B).
Perceptual size asymmetry threshold
The response of birds presented with one butterfly with two
equal-sized spots and one butterfly with an asymmetric signal
consisting of two different-sized spots suggests that the
protective value of avoidance-inducing signals is impaired by
asymmetry in the size of pattern elements. In the treatment
with a mean spot-size asymmetry of 5%, butterflies with
asymmetric signals were attacked at the same rate as those
with symmetric signals (two-tailed binomial test, z ¼ 0.22, p ¼
.91), whereas the size-asymmetric butterflies suffered a significantly higher rate of food-crumb removal than did symmetric
butterflies in all treatments with a spot-size asymmetry of 7.5%
or more (7.5%: z ¼ 2.80, p ¼ .0038; 10%: z ¼ 3.24, p ¼ .0014;
15%: z ¼ 3.46, p ¼ .0006; 33%: z ¼ 3.02, p ¼ .0026) (Figure 5).
The relative rate of food-crumb removal from butterflies with
size-asymmetric signals did not increase progressively across
treatments with increasing degree of asymmetry (rs ¼ .45, n ¼
5 treatments, p ¼ .45) but instead followed a step function
(Figure 5), a finding consistent with expectations from the
hypothesis of a threshold for asymmetry detection and
response beyond which further increments in asymmetry
levels have no influence on signal efficacy.
DISCUSSION
In summary, birds showed stronger spontaneous aversions to
artificial butterflies possessing symmetric coloration than to
Forsman and Herrström
•
Signal asymmetry and predation risk
145
Figure 5
Proportion of asymmetric signaling butterflies with one large and one
small yellow spot from which the food crumbs were first removed
when presented together with symmetric signaling butterflies with two
equal-sized yellow spots in experiment 6. The values along the abscissa
are degree of bilateral spot-size asymmetry, expressed as a percentage
of spot diameter. They represent a continuum from nearly symmetric
(far left) to very asymmetric (far right). The dotted reference line
indicates equal rate of food-crumb removal for the symmetric and
asymmetric signal type. Symbols above bars indicate results from twotailed binomial tests for large samples. n.s. indicates not significant.
**p , .01; ***p , .001.
Figure 4
Rate of food-crumb removal for signaling butterflies with different
shapes of the signaling pattern elements. The symbols along the
abscissa indicate the shapes of the two signaling pattern elements on
each of the two prey types presented together. (a) The two bars to
the left indicate the comparison between two symmetric signal types
used in experiment 3. The two right bars indicate the comparison
between one symmetric and one asymmetric signal used in
experiment 4. (b) Comparison of rate of food-crumb removal for
prey with asymmetric signals consisting of one cross and one bar
when presented together with symmetric signals consisting either of
two crosses (two left bars) or two bars (right bars). Results are from
experiment 5. Symbols above bars indicate results from two-tailed
binomial tests. *p , .05; **p , .01.
butterflies with asymmetries in color, shape, or size of the
signaling pattern elements. These findings are consistent with
the hypothesis (Forsman and Merilaita, 1999; Kirkpatrick and
Rosenthal, 1994; Møller and Swaddle, 1997) that the protective
value of conspicuous prey color patterns is impaired by
asymmetry.
The response of birds presented simultaneously with
a monochromatic butterfly and a butterfly with signaling
spots differed depending on the color of the spots. Although
birds showed no aversion to butterflies with blue or red spots,
they avoided yellow spots and showed a weak attraction (albeit
not statistically significant) to white spots. These findings
highlight the variable influence of different colors on
unconditioned aversions (see also Coppinger, 1969; 1970;
Osorio et al., 1999). The unconditioned avoidance of
butterflies with yellow spots further suggests that a deviant
mutant, such as a conspicuously colored prey, does not
necessarily suffer high predation from naive predators as
a result of an increased probability of detection (Endler, 1991;
Götmark, 1994; Lindström et al., 1999).
Although experiment 1 uncovered variable effects on
unconditioned aversion of color per se, color symmetry seems
to be even more important. Thus, in the second treatment of
experiment 2, butterflies with one white spot and one yellow
spot suffered a significantly higher rate of removal than did
butterflies with two white spots. Because the results from
experiment 1 revealed that birds significantly avoided yellow
but not white spots, the latter result must reflect a negative
effect of color asymmetry on avoidance-inducing signaling,
rather than an effect of color per se. In the first treatment,
butterflies with one red spot and one yellow spot were
attacked at the same rate as were color symmetric butterflies
with two red spots. Viewed alone, this result may be owing to
equal aversion (or attraction) to red and yellow. However,
given that the birds in experiment 1 avoided yellow but not
red spots, the finding that birds in experiment 2 showed no
aversion to butterflies with one yellow spot and one red spot is
consistent with the hypothesis that color asymmetry impairs
the protective value of conspicuous coloration. In a previous
investigation of the role of color asymmetry on sexual
signaling, Swaddle and Cuthill (1994) found that female
zebra finches chose color-symmetric leg-banded males over
color-asymmetric banded ones (see also Fiske and Amundsen,
1997). Thus, although color symmetry seems to make warning
signals more aversive, it appears to increase the attractiveness
of secondary sexual ornaments. Taken together, these
findings argue against the notion (for review, see Swaddle,
1999a) that organisms have inherent general preferences
for symmetry over asymmetry, and suggest instead that
receivers’ responses to color-asymmetric signals are context
specific.
The finding that butterflies with a signal consisting of two
circular pattern elements experienced a lower rate of foodcrumb removal than did butterflies with two squares may
reflect a stronger avoidance of more eyelike objects (Coppinger, 1969, 1970; Tinbergen, 1974). Despite the stronger
aversion induced by circular compared with squared pattern
elements, however, shape-asymmetric butterflies with one spot
and one square suffered a significantly higher rate of foodcrumb removal than did symmetric butterflies with two
squares. A similar negative effect of shape asymmetry on
avoidance was evident among birds presented with novel
pattern elements not normally found in nature. It thus seems
that the protective value of conspicuous coloration is
impaired not only by color asymmetry but also by asymmetries
Behavioral Ecology Vol. 15 No. 1
146
in shape of the signaling pattern elements. This latter finding
suggests that the high degree of bilateral symmetry in shape of
color pattern elements characteristic of most species of
animals (Wallace 1889) may reflect not only developmental
constraints but also selection against asymmetric phenotypes
imposed by visually oriented predators (Forsman and
Merilaita, 1999).
The mean asymmetry in natural populations typically
constitutes only 1–2% of trait size, and it has been suggested
that most individuals may be perceived as symmetric and that
asymmetry may play no role in signaling (Swaddle, 1999a).
However, the degree of asymmetry varies both among
characters and individuals. For instance, analyses of asymmetry in color pattern elements on the wings of three species of
moths (Arctia caja L., Noctua orbona (L., Smerinthus ocellata L.)
showed that mean asymmetries constituted 4.3% (range ¼
2.1–7.0%) of trait size, whereas individual asymmetry levels
reached as high as 26% (Forsman and Merilaita, 2003).
Swaddle (1999b) showed that European starlings could
accurately discriminate 1.8% asymmetry from symmetry, but
were unable to discriminate 1.25% asymmetric stimuli from
symmetric patterns. Similarly, we found that birds attacked
butterflies with a spot-size asymmetry of 5% at the same rate as
those with symmetric signals, whereas the size-asymmetric
butterflies suffered a significantly higher rate of food-crumb
removal than did symmetric butterflies in all treatments with
a spot-size asymmetry of 7.5% or more. Interestingly, birds’
avoidance of symmetric signals did not increase progressively
across treatments as a function of the degree of spot-size
asymmetry, but the variation among treatments instead
followed a step-function. These results are consistent with
the idea (Schwabl and Delius, 1984; Swaddle, 1999b) of
a perceptual asymmetry threshold beyond which increased
asymmetry levels have no or little influence on signal efficacy.
Because our experiments measured unconditioned avoidance
only, with no learning being involved (unlike the experimental design used by Swaddle [1999b], which did incorporate
learning), the observed threshold in our experiment may be
an overestimate of the true detection threshold and represent
instead a response threshold. Collectively, these results
nevertheless suggest that at least in some species of butterflies
and moths, the magnitude of individual differences in size
asymmetry of color patterns exceeds the asymmetry detection
threshold in birds and, hence, may be influenced by selective
predation.
Conspicuous coloration typically occurs in animals that are
distasteful, noxious, or otherwise dangerous to potential
predators (Cott, 1940; Endler, 1991; Gittleman and Harvey,
1980; Guilford and Dawkins, 1991; Summers and Clough,
2001; Wallace, 1867). However, we measured the spontaneous
and initial response of naive predators, with no learning or
unpalatability being involved. The stronger aversions toward
symmetric color patterns as revealed by our experiments
thus suggest that a high degree of symmetry in color, shape,
and size of color pattern elements may decrease susceptibility
of conspicuous prey (even if they have no chemical or
structural defense mechanisms) to inexperienced predators,
as well as enhance the survival prospects of rare mutant
aposematic phenotypes. The influence of asymmetry on the
evolution of conspicuous color patterns will be even greater if
it proves to negatively influence also the ability of predators
to learn and associate visual warning signals with unpalatability.
We thank Ingemar J. for immense help with the birds, and J. Ahnesjö,
E. Civantos, L. Lindström, and S. Ulfstrand for helpful comments on
an earlier version of the manuscript. The study was supported by the
Swedish Natural Science Research Council (grant to A.F.), Växjö
University, and Kalmar University.
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