Pattern mimicry of host eggs by the Common Cuckoo, as seen through a bird's eye

Abstract

Cuckoo-host interactions provide classical examples of coevolution. Cuckoos place hosts under selection to detect and reject foreign eggs, while host defences result in the evolution of host-egg mimicry in cuckoos. Despite a long history of research, egg pattern mimicry has never been objectively quantified, and so its coevolution with host defences has not been properly assessed. Here, we use digital image analysis and modelling of avian vision to quantify the level of pattern mimicry in eight host species of the common cuckoo Cuculus canorus and their respective cuckoo host-races. We measure a range of pattern attributes, including marking size, diversity in size, contrast, coverage and dispersion. This new technique reveals hitherto unnoticed sophistication in egg pattern mimicry. We show that various features of host egg pattern are mimicked by the eggs of their respective cuckoo host-races, and that cuckoos have evolved better pattern mimicry for host species that exhibit stronger egg rejection. Pattern differs relatively more between eggs of different host species than between their respective cuckoo host-races. We suggest that cuckoos may have more 'average' markings in order to be able to use subsidiary hosts. Our study sheds new light on cuckoo-host coevolution and illustrates a new technique for quantifying animal markings with respect to the relevant animal visual system.

Full text

Pattern mimicry of host eggs by the common
cuckoo, as seen through a bird’s eye
Mary Caswell Stoddard*and Martin Stevens
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
Cuckoo–host interactions provide classical examples of coevolution. Cuckoos place hosts under selection
to detect and reject foreign eggs, while host defences result in the evolution of host-egg mimicry in cuck-
oos. Despite a long history of research, egg pattern mimicry has never been objectively quantified, and so
its coevolution with host defences has not been properly assessed. Here, we use digital image analysis and
modelling of avian vision to quantify the level of pattern mimicry in eight host species of the common
cuckoo Cuculus canorus and their respective cuckoo host-races. We measure a range of pattern attributes,
including marking size, diversity in size, contrast, coverage and dispersion. This new technique reveals
hitherto unnoticed sophistication in egg pattern mimicry. We show that various features of host egg pat-
tern are mimicked by the eggs of their respective cuckoo host-races, and that cuckoos have evolved better
pattern mimicry for host species that exhibit stronger egg rejection. Pattern differs relatively more between
eggs of different host species than between their respective cuckoo host-races. We suggest that cuckoos
may have more ‘average’ markings in order to be able to use subsidiary hosts. Our study sheds new
light on cuckoo – host coevolution and illustrates a new technique for quantifying animal markings with
respect to the relevant animal visual system.
Keywords: pattern mimicry; brood parasitism; bird vision; egg rejection; cuckoos; digital image analysis
1. INTRODUCTION
Brood parasitic birds lay their eggs in the nest of another
species, so that the parasitized parents rear the foreign
young to fledging (Davies 2000). Coevolution between
brood parasites and their hosts provides many classical
examples of evolutionary arms races, whereby selection
pressure imposed by parasitism leads to host adaptations
to detect and reject parasitic young, and to parasite coun-
ter-adaptations, such as egg mimicry (Rothstein 1990).
Arguably, the most extensively studied brood parasite is
the common cuckoo Cuculus canorus, which comprises
several different host-races or gentes, with each female
cuckoo specializing on a particular host species. To
human eyes, females of a given gens often (but not
always) lay an egg that mimics the appearance of the
host egg in both colour and pattern, because many
hosts have evolved the ability to discriminate accurately
between their own and a foreign egg (Brooke & Davies
1988).
Although there have been a number of studies of egg
mimicry in brood parasites, especially common cuckoos
(e.g. Brooke & Davies 1988;Davies & Brooke 1989),
the vast majority of work has been based on human
assessments of colour and pattern, despite the well-
known differences between human and avian vision
(Bennett et al. 1994). Recently, several studies have
analysed the level of match between foreign and host
eggs using models of avian colour and luminance visual
discrimination (Avile
´s 2008;Cassey et al. 2008;
Langmore et al. 2009). Such models more accurately
predict differences in egg appearance and egg rejection
behaviour in hosts than do human assessments and can
‘revolutionize the investigation of host– brood parasite
relationships’ (Safran & Vitousek 2008). However, pre-
vious work indicates that pattern also plays a crucial
role in egg rejection in a range of brood parasitic systems
(e.g. Lahti & Lahti 2002;Lo
´pez-de-Hierro & Moreno-
Rueda in press). While many biologists have adopted
methods of studying the colour and luminance of visual
signals from the correct receiver’s perspective (or at least
objectively), it is still strikingly rare to find quantifications
of animal patterns not based on human subjective assess-
ment (but see for example: Godfrey et al. 1987;Stevens &
Cuthill 2006;Barbosa et al. 2008). Analyses of egg pat-
tern have almost always been based on human vision,
with quantification of egg markings based on human-
produced ordinal rankings of spottiness or dispersion,
either from the eggs themselves (e.g. Davies & Brooke
1989;Moksnes & Røskaft 1995;Gosler et al. 2000)or
based on apparently uncalibrated photographs (e.g.
Nguyen et al. 2007;Sanz & Garcı
´a-Navas 2009). Just as
human subjective assessments of visual signals are inap-
propriate with respect to colour and luminance (Bennett
et al. 1994;Safran & Vitousek 2008), the same is likely
to be true for pattern. The lack of research into the func-
tion of the two- or three-dimensional patterning of
markings on an object represents a key shortcoming
of current work on visual signals. Common methods used
to obtain objective colour information (e.g. reflectance
spectrometry) are unsuited to the task of capturing complex
patterns (Stevens et al.2007), yet advances in digital pho-
tography, computer vision and image-processing now
provide a suite of ideal techniques to quantify objectively
two-dimensional visual signals, and can be analysed in
conjunction with specific models of visual processing
*Author for correspondence (mcs66@cam.ac.uk).
Electronic supplementary material is available at http://dx.doi.org/10.
1098/rspb.2009.2018 or via http://rspb.royalsocietypublishing.org.
Proc. R. Soc. B (2010) 277, 1387–1393
doi:10.1098/rspb.2009.2018
Published online 6 January 2010
Received 4 November 2009
Accepted 8 December 2009 1387 This journal is q2010 The Royal Society

(Godfrey et al.1987;Stevens & Cuthill 2006;Stevens et al.
2007).
Here, for the first time, to our knowledge, we use
methods based on avian visual perception and digital
image analysis to quantify egg pattern mimicry between a
brood parasite and its main hosts. We do this in the
common cuckoo and eight of its principal hosts, and
investigate the extent to which the level of pattern match
between cuckoo and host eggs can be explained by host
rejection rates reported in the literature (Avile
´s&
Garamszegi 2007).
2. MATERIAL AND METHODS
(a)Data collection
We photographed 205 parasitized clutches of host eggs held
in the Natural History Museum (NHM; Tring, Hertfordshire,
UK), with clutches belonging to eight principal cuckoo hosts
in Europe: great reed warbler (Acrocephalus arundinaceus,
n¼27: all from Hungary), reed warbler (Acrocephalus
scirpaceus,n¼29: all from England), meadow pipit (Anthus
pratensis,n¼30: all from England), brambling (Fringilla
montifringilla,n¼13: 12 from Finland, 1 Russia), red-
backed shrike (Lanius collurio,n¼26: 16 from Germany,
6 England, 2 Czech Republic, 1 Hungary, 1 Pomerania),
pied wagtail (Motacilla alba,n¼28: all from England), dun-
nock (Prunella modularis,n¼30: all from England) and
garden warbler (Sylvia borin,n¼22: 10 from Germany, 6
England, 2 Czech Republic, 2 Pomerania, 1 France, 1
Poland). Almost all eggs were collected between 1880 and
1940, with more than half collected between 1880 and
1910. Egg pigmentation may be affected by fading or vari-
able environmental conditions (Avile
´set al. 2007).
However, the effects of these potential sources of bias were
probably limited because eggs (i) were stored in the dark
under controlled conditions to minimize fading, and (ii)
were sampled from many different localities and in different
years. To avoid measuring more than one cuckoo egg laid
by the same female, we selected clutches from different
localities. When overlap by locality was unavoidable, we
only used clutches obtained several years apart or by different
collectors. We photographed the entire clutch, but randomly
chose one host egg per clutch for subsequent analyses.
(b)Image acquisition and calibration
Images were taken with a Fujifilm IS Pro ultraviolet (UV)-
sensitive digital camera with a quartz CoastalOpt UV lens
(Coastal Optical Systems), fitted with a UV and infrared
(IR) blocking filter for photographs in the human visible
spectrum (Baader UV/IR Cut filter; transmitting between
400 and 700 nm), and with a UV pass filter (Baader U
filter; transmitting between 300 and 400 nm) for the UV
images. Each image included a Spectralon grey reflectance
standard (Labsphere, Congleton, UK), reflecting light
equally at 40 per cent between 300 and 750 nm. All images
were taken at the same distance and angle from the eggs,
and therefore all markings were at the same scale. Two UV-
emitting lamps (Kaiser RB260 Digital Lighting Unit) kept
at a fixed distance from the eggs provided standard, constant
illumination. Each image was linearized with respect to light
intensity, because most cameras show a nonlinear response in
image value with changes in radiance (see Stevens et al.
(2007) for details). Generally, perception of pattern and tex-
ture is primarily a function of achromatic (luminance) vision;
in birds, evidence indicates that luminance is encoded by the
double cones (Jones & Osorio 2004;Osorio & Vorobyev
2005). Therefore, we analysed pattern just in terms of this
luminance channel, but also undertook analysis to confirm
that we were not missing pattern information in other parts
of the avian visible spectrum (see electronic supplementary
material). Since we know the spectral sensitivity of our
camera set-up (M. Stevens 2007, unpublished data), the
images were transformed from camera colour space to corre-
spond to the relative photon catches of a bird’s double cones
(Stevens & Cuthill 2006;Stevens et al. 2007), using the spec-
tral sensitivity of a blue tit Cyanistes caeruleus (Hart et al.
2000). The blue tit is a relatively well studied bird in terms
of its visual system, and seems representative of most
higher passerines (Hart & Hunt 2007). All calibrations and
pattern analyses were undertaken with self-written pro-
grammes in MATLAB
1
(The MathWorks, Inc., MA, USA)
and its associated Image Processing toolbox.
For each image of an egg, we extracted three sub-images
of equal size (sizes identical across all eggs analysed), corre-
sponding to the upper, middle and base sections (thirds) of
the eggs. We initially analysed these regions separately
because characteristics of the markings can vary across
these regions, with markings usually densest at the base.
(c)Pattern analysis: granularity
To analyse the pattern sizes and contrasts of the egg markings,
we adopted a ‘granularity’ analysis similar to that recently
used to analyse cuttlefish camouflage markings (Barbosa
et al. 2008;Chiao et al. 2009), which is ideal for analysing
the contribution that different marking sizes make to a given
pattern. For each calibrated image of an egg region, we pro-
duced seven new images, each containing information at
different spatial scales, by fast Fourier transforming the orig-
inal image (Godfrey et al. 1987) and applying seven octave-
wide, isotropic band-pass filters (Barbosa et al. 2008).
These filters function like a sieve, capturing information at
different spatial scales (different sized markings), with smaller
filter sizes corresponding to larger (low spatial frequency)
markings and larger filter sizes corresponding to smaller
(high spatial frequency) markings. Although real visual sys-
tems do not directly filter spatial information in the same
way as a Fourier transform, early-stage visual processing
does break down information in a scene into different spatial
frequencies by virtue of receptive fields (Campbell & Robson
1968;Godfrey et al. 1987). Adding together the seven differ-
ent filtered images produces a new image that is a close
approximation to the original unfiltered image, with only a
small loss of information. Analysing these seven different
images (‘granularity bands’; Barbosa et al. 2008) allows us
to determine the relative contribution of different marking
sizes to the overall egg pattern, and to quantify the level of
match of each cuckoo gens and host.
After filtering an image, we calculated a range of pattern
information. First, for each granularity band (1 – 7), we cal-
culated the overall pattern ‘energy’ (e), as the sum of the
squared pixel values in each image divided by the number
of pixels in the image, with the actual scale being arbitrary
(Chiao et al. 2009). The values of eacross all seven band-
pass filtered images produce a ‘granularity spectrum’
(Chiao et al. 2009). From each granularity spectrum, we
can calculate a range of information about an egg’s markings.
First, we calculated the maximum value of ein the spectrum
(maximum energy; e
max
), as the filter size containing the
1388 M. C. Stoddard & M. Stevens Pattern mimicry of host eggs by cuckoo
Proc. R. Soc. B (2010)

highest energy, which thus corresponds to the predominant
marking size. We also calculated the proportion of the total
energy across all scales corresponding to e
max
(proportion
energy; e
prop
). This value provides a measure of how impor-
tant the main marking size is to the overall egg pattern; a high
value indicates that the egg pattern is dominated by this
marking size. The total energy (e
tot
) across all filter sizes cor-
responds to the overall amplitude of the spectrum, and
provides a measure of overall pattern contrast (Chiao et al.
2009), with higher values indicating more contrasting
markings.
(d)Pattern analysis: pattern coverage and dispersion
In addition to the granularity analysis, we calculated the rela-
tive proportion of each egg region covered by markings. To
do this, we thresholded the calibrated images into a binary
format, with a pixel value of one corresponding to a marking
and zero to the background egg colour. Although it would
have been ideal to threshold each image automatically/adap-
tively, deviations in ambient lighting and the curvature of the
egg (even on the relatively ‘flatter’ regions selected) pre-
vented this, with this approach producing highly inaccurate
representations of pattern. We interactively chose a thresh-
olding value that, to the human eye, reproduced the egg
pattern coverage. Although this introduces some subjectivity,
any error associated should be minor because: (i) there
should be no bias towards a particular direction of marking
coverage; (ii) patterns in the UV not represented in the ana-
lysed images coincided with the human visible pattern; and
(iii) the actual values for pattern coverage were calculated
from the thresholded images, and not by human eye. Pattern
coverage was calculated as the proportion of the pixels corre-
sponding to a marking (values of one) compared with the
overall image size (total number of pixels). In addition, we
calculated pattern dispersion, described by the standard
deviation of pattern coverage for each of the three egg
regions. A low standard deviation indicates uniform pattern
coverage across the egg, while a high value indicates that
one or two regions are disproportionately covered by
markings.
(e)Statistical methods
For each cuckoo and host egg, we calculated marking filter
size (e
max
), proportion energy (e
prop
), total energy (e
tot
) and
pattern coverage for each egg region (upper, middle, base),
in addition to overall pattern dispersion among regions.
Initial analyses indicated that differences between egg regions
were minor for marking filter size, proportion energy and
total energy (electronic supplementary material, figure S1).
Consequently, we averaged these upper, middle and base
measurements for each egg to yield overall measures of egg
pattern and contrast. These different pattern attributes are
not highly correlated with each other (electronic supplemen-
tary material, table S1). One-way analysis of variances tested
whether eggs of cuckoo gentes differ significantly for each
measure of pattern.
We then compared the values of cuckoos and hosts to
assess egg pattern mimicry for each attribute. Following
Nakagawa & Cuthill (2007), we determined the magnitude
of difference between patterns for each cuckoo – host
pair, and calculated Cohen’s d(standardized mean
difference) with regard to each pattern measure (Cohen
1988). Cohen’s dis an effect size measure used to describe
the overlap of distributions, with larger effect sizes indicating
a smaller overlap. Following Cohen’s (1988) description
of ‘large’ effects (d¼0.8), we determined whether
cuckoo–host pairs ‘matched’ (d,0.8) for each pattern
attribute.
Interval plots illustrate the degree of overlap for cuckoos
and hosts for each measure (see electronic supplementary
material, figures S2 and S3). To determine if variation
between cuckoo and host eggs differed for each pattern
attribute, we used Levene’s tests for equal variances.
Finally, we compared overall pattern mimicry to previously
established rejection rates of non-mimetic eggs by hosts.
Since the likelihood of rejection can vary depending on
the context (such as being affected by the rate of parasitism
in the population or the experience of the host; Davies
2000), we refer both to rates measured directly by
Davies & Brooke (1989) and to rates calculated from several
published and unpublished sources compiled in Avile
´s&
Garamszegi (2007). When plotting rejection rate versus
pattern-matching, we use rates calculated by Avile
´s&
Garamszegi (2007) only, since this study alone provides
rejection rates for all eight hosts.
3. RESULTS
There were significant differences between cuckoo egg-
morphs for all five variables measured (electronic
supplementary material, table S2): marking filter size
(F
7,197
¼2.18, p¼0.038), proportion energy (F
7,197
¼
2.64, p¼0.012), total energy (F
7,197
¼11.92, p,
0.001), pattern coverage (F
7,197
¼23, p,0.001), and
pattern dispersion (F
7,197
¼2.74, p¼0.01). Variation
among host eggs was higher than the variation among
the cuckoo gentes for all five pattern attributes (n¼205
for both hosts and cuckoo; electronic supplementary
material, table S3): marking filter size (W¼13.77, p,
0.001), proportion energy (W¼10.14, p¼0.002), total
energy (W¼34.75, p,0.001), pattern coverage (W¼
41.47, p,0.001), and pattern dispersion (W¼8.14,
p¼0.005). Granularity profiles revealed varying degrees
of matching between cuckoo and host eggs, with the
shape and amplitude of the cuckoo granularity spectrum
yielding a nearly identical match to its host in some
instances (i.e. brambling) but deviating considerably in
others (see figure 1 and §4). Magnitudes of difference
(Cohen’s dvalues) showed the extent to which cuckoo
and host distributions overlap for each pattern variable,
with cuckoo patterns matching certain features of host
pattern better than others (table 1). A comparison of
egg pattern mimicry to host rejection data (Avile
´s&
Garamszegi 2007) indicated that mimicry improves with
increasingly strong host rejection (figure 2).
The absence of egg pattern mimicry is most striking in
the dunnock, which rejects non-mimetic eggs at low rates
ranging from 2 per cent (Avile
´s & Garamszegi 2007)to6
per cent (Davies & Brooke 1989). The lack of pattern
mimicry is evident in the divergent granularity profiles
of the cuckoo and host (figure 1d), and because the dun-
nock-cuckoo egg matches its host in only one of the
five pattern characteristics (table 1). Cuckoos parasitizing
the meadow pipit, with moderate rejection rates between
18 per cent (Avile
´s & Garamszegi 2007) and 48 per cent
(Davies & Brooke 1989), lay eggs that match host pattern
in two categories: marking size and pattern dispersion
(table 1), and have granularity profiles only roughly
Pattern mimicry of host eggs by cuckoo M. C. Stoddard & M. Stevens 1389
Proc. R. Soc. B (2010)

following the host spectrum shape (figure 1e). The reed
warbler also has moderate egg rejection rates, from
31 per cent (Avile
´s & Garamszegi 2007) to 62 per cent
(Davies & Brooke 1989), and its corresponding cuckoo
egg matches the host pattern in marking size and
proportion energy (table 1). Granularity profiles match
in general shape, particularly at higher filter sizes (i.e.
smaller markings; figure 1b). Cuckoos parasitizing the
garden warbler, with a high rejection rate of 67 per cent
(Avile
´s & Garamszegi 2007), match the host pattern in
cuckoo host cuckoo host
cuckoo host
cuckoo host
cuckoo host cuckoo host
cuckoo host
cuckoo host
filter size filter size
600(a)
(b)( f )
(c)(g)
(h)(d)
(e)
500
Great reed warbler
Acrocephalus arundinaceus
Meadow pipit
Anthus pratensis
Reed warbler
Acrocephalus scirpaceus
Brambling
Fringilla montifringilla
Dunnock
Prunella modularis
Garden warbler
Sylvia borin
Red-backed shrike
Lanius collurio
Pied wagtail
Motacilla alba
400
300
200
100
0
400
350
300
250
normalized energynormalized energynormalized energy normalized energy
200
200
180
160
140
120
100
160
140
120
100
80
60
40
20
0 5 10 15 20 25 30 35 40 45 50 55 60 65 5 101520253035404550556065
80
60
40
20
0
150
100
50
0
300
250
200
150
100
50
0
300
250
200
150
100
50
0
200
220
180
160
140
120
100
80
60
40
20
0
80
70
60
50
40
30
20
10
0
Figure 1. Average granularity spectra for each host (grey lines) and its respective cuckoo gens (black lines), illustrating the
contribution of different marking sizes to the given pattern. Measurements were made at the following filter sizes: 1, 2, 4, 8,
16, 32, 64. Granularity profiles show varying degrees of match between cuckoo and host eggs, with the shape and amplitude
of the cuckoo granularity spectrum yielding a nearly identical match to its host in some instances (e.g. brambling) but no match
in others (e.g. dunnock). We averaged the top, middle and base spectra for each egg to yield overall measures of egg pattern and
contrast (electronic supplementary material, figure S1). Photographs of eggs within the figure are copyright of the NHM and
were taken by Mary Caswell Stoddard.
1390 M. C. Stoddard & M. Stevens Pattern mimicry of host eggs by cuckoo
Proc. R. Soc. B (2010)

marking size, pattern coverage and pattern dispersion
(table 1), but have a poor match in contrast (figure 1h).
The great reed warbler rejects non-mimetic eggs at a
high rate of 88 per cent (Avile
´s & Garamszegi 2007),
and its cuckoo gens matches host egg pattern in marking
size, proportion energy and pattern dispersion (table 1),
and matches the host granularity spectra well in shape,
particularly at higher filter sizes (figure 1a). The pied
wagtail-cuckoo matches the marking size, proportion
energy and pattern dispersion of eggs laid by the host,
which has rejection rates ranging from 71 per cent
(Davies & Brooke 1989) to 91 per cent (Avile
´s&
Garamszegi 2007). The granularity profile of the cuckoo
matches the shape of the host spectrum but not the ampli-
tude (figure 1g). The red-backed shrike shows strong
rejection (100%, Avile
´s & Garamszegi 2007), and its
cuckoo matches the host in marking size, proportion
energy and total contrast, but not pattern coverage or dis-
persion (table 1). This is because the cuckoo egg rarely
mimics the ‘corona’ ring of markings that is prominent at
the middle of red-backed shrike eggs. The granularity pro-
files match very closely for all but two of the sizes
(figure 1c). In accordance with strong rejection shown by
the brambling (90%, Avile
´s & Garamszegi 2007), its
cuckoo matches the host eggs across all five pattern charac-
teristics (table 1), with the granularity spectra essentially
identical (figure 1f).
4. DISCUSSION
Here, we quantified five different characteristics of egg
pattern mimicry between the common cuckoo and
eight of its principal hosts, and revealed varying degrees
of matching between each cuckoo gens and host
(figure 1). Previous studies using subjective human cri-
teria have usually focused on a basic ‘matching’ score,
which ignores the relative contribution of different pat-
tern attributes to overall pattern mimicry. Our
technique demonstrates that pattern is composed of
multiple different attributes (e.g. marking size, dispersion,
etc.) that should be considered independently. Further-
more, different components of a pattern may be
relatively more important in general (across most species),
such as marking size, whereas other characteristics appear
to be more important to different host species in achieving
mimicry (table 1). Our analyses support the conclusion
that cuckoos have evolved better mimetic egg patterns
where host species show strong egg rejection (figure 2).
In addition, there are significant differences in pattern
among the cuckoo gentes (electronic supplementary
material, table S2), but cuckoos have significantly less
diverse patterns than hosts.
Gentes of the common cuckoo and their hosts appear
to be at various stages of an evolutionary arms race, in
which the cuckoo’s match to host eggs improves as the
hosts evolve better rejection defences (Davies 2000).
Early studies indicated that cuckoos lay a better mimetic
egg where the host species is more discriminating
(Brooke & Davies 1988;Davies & Brooke 1989). Our
pattern analyses support this. The cuckoo has no pattern
mimicry where the hosts show no rejection, moderate pat-
tern mimicry where the hosts show modest rejection, and
excellent pattern mimicry with strong host rejection
(figure 2). The cuckoo gentes match the predominant
marking size for all hosts except the dunnock, suggesting
that a good match in marking size is crucial for evolving
mimetic eggs across species. However, differences in the
nature and extent of pattern-matching suggest that differ-
ent hosts may rely on different pattern attributes in
rejecting eggs, with more sophisticated mimicry achieved
when the cuckoo egg matches not only marking size but
also more nuanced aspects of pattern. Whereas previous
studies have often treated pattern as a single entity (e.g.
Brooke & Davies 1988;Nguyen et al. 2007), our results
demonstrate that some cues (e.g. marking size) may be
relatively more important in general, with others used dif-
ferentially across host species. Some species, such as the
dunnock, fail to reject cuckoo eggs in spite of low pat-
tern-matching and high fitness consequences of
rejection, possibly because dunnocks are in an earlier
stage of the arms race with the cuckoo and the lack of
egg rejection may be owing to a time lag in developing
host defences (Davies & Brooke 1989). In other host
species, lack of rejection may stem from costs associated
with recognition errors, or if hosts cannot see the eggs;
for example, some hosts of Australian bronze-cuckoos,
Chalcites, do not reject dark-coloured cuckoo eggs that
look very different from the host eggs, possibly because
the cuckoo eggs are well camouflaged in the nest
(Langmore et al. 2009).
We found statistically significant differences between
the cuckoo gentes for all pattern characteristics measured
(electronic supplementary material, table S2), corrobor-
ating the existence of distinct cuckoo egg-morphs for
Table 1. Summary of the magnitudes of difference (Cohen’s dvalues, standardized mean difference) between egg pattern
attributes for each cuckoo gens and its host. (Small dvalues indicate a large overlap of distributions, while large dvalues
indicate a small overlap. Following Cohen (1988), we considered smaller effect sizes (d,0.8) to indicate ‘matches’ between
cuckoo and host patterns, shown here in bold and italics.)
host n
marking filter size;
log-transformed
proportion
energy total energy
pattern
coverage
pattern
dispersion
great reed warbler 27 0.0080 0.6631 0.8960 0.8963 0.0192
reed warbler 29 0.0898 0.6338 1.0538 1.5319 0.9430
meadow pipit 30 0.0814 1.0509 1.5535 1.7613 0.0641
brambling 13 0.5819 0.1483 0.2135 0.1534 0.2805
red-backed shrike 26 0.1675 0.7851 0.4488 0.9743 1.1477
pied wagtail 28 0.4207 0.3669 1.3111 1.8642 0.0952
dunnock 30 2.9727 0.2005 1.7698 6.6545 2.0360
garden warbler 22 0.1363 1.4256 1.1021 0.0999 0.0076
Pattern mimicry of host eggs by cuckoo M. C. Stoddard & M. Stevens 1391
Proc. R. Soc. B (2010)

the eight gentes studied (Moksnes & Røskaft 1995;
Davies 2000). Interestingly, our analyses showed that
the eggs of the different cuckoo gentes were significantly
less variable than were the host eggs. A more general pat-
tern could permit cuckoos to parasitize subsidiary hosts
successfully when the primary host is unavailable
(Brooke & Davies 1991;Moksnes & Røskaft 1995).
Alternatively, the relative similarity of cuckoo eggs could
result from genetic constraints on egg-patterning in
cuckoos or from evolutionary lag (Davies 2000).
To date, few experiments have established which visual
cues are important in determining egg rejection behaviour
by hosts (but see Polac
ˇikova
´et al. 2007;Moska
´tet al.
2008), partly stemming from the lack of consistent
methods for quantifying egg appearance. Future tests
must incorporate pattern, measured either objectively or
through a bird’s own eyes. Of course, pattern should
not be considered in isolation: selection has acted on
egg size, shape, colour, luminance and pattern simul-
taneously, and these cues together contribute to egg
detection and rejection behaviour. Overall, to understand
the form and evolution of visual signals and how they
relate to behaviour, we should further incorporate the
spatial component of animal markings in future work.
We thank the editor T. Price and two anonymous referees for
a range of helpful comments and suggestions. We also thank
Douglas Russell, Robert Prys-Jones and the staff of the
NHM, Tring, for kindly allowing access to collections, and
Nick Davies and Rebecca Kilner for a range of advice.
M.C.S. was supported by a Marshall Scholarship, the
Cambridge Overseas Trust, and the Hanne and Torkel
Weis-Fogh Fund. M.S. was supported by a Biotechnology
and Biological Sciences Research Council David Phillips
Fellowship (BB/G022887/1) and Girton College,
Cambridge.
ENDNOTE
1
MATLAB functions for undertaking the pattern analysis outlined in
this paper are available from M.S. (ms726@cam.ac.uk).
REFERENCES
Avile
´s, J. M. 2008 Egg colour mimicry in the common
cuckoo Cuculus canorus as revealed by modelling host reti-
nal function. Proc. R. Soc. B 275, 2345 – 2352. (doi:10.
1098/rspb.2008.0720)
Avile
´s, J. M. & Garamszegi, L. Z. 2007 Egg rejection and
brain size among potential hosts of the common cuckoo.
Ethology 113, 562–572. (doi:10.1111/j.1439-0310.2007.
01359.x)
Avile
´s, J., Stokke, B., Moksnes, A., Røskaft, E. & Møller, A.
2007 Environmental conditions influence egg color of reed
warblers Acrocephalus scirpaceus and their parasite, the
common cuckoo Cuculus canorus.Behav. Ecol. Sociobiol.
61, 475 – 485. (doi:10.1007/s00265-006-0275-0)
Barbosa, A., Ma¨thger, L. M., Buresch, K. C., Kelly, J.,
Chubb, C., Chiao, C.-C. & Hanlon, R. T. 2008 Cuttlefish
camouflage: the effects of substrate contrast and size in
evoking uniform, mottle or disruptive body patterns.
Vis. Res. 48, 1242– 1253. (doi:10.1016/j.visres.2008.
02.011)
Bennett, A. T. D., Cuthill, I. C. & Norris, K. J. 1994 Sexual
selection and the mismeasure of color. Am. Nat. 144,
848–860. (doi:10.1086/285711)
Brooke, M. de L. & Davies, N. B. 1988 Egg mimicry by
cuckoos Cuculus canorus in relation to discrimination by
hosts. Nature 335, 630– 632.
Brooke, M. de L. & Davies, N. B. 1991 A failure to demon-
strate host imprinting in the cuckoo (Cuculus canorus) and
alternative hypotheses for the maintenance of egg mimi-
cry. Ethology 89, 154– 166.
Campbell, F. W. & Robson, J. G. 1968 Applications of Four-
ier analysis to the visibility of gratings. J. Physiol. 197,
551–556.
Cassey, P., Honza, M., Grim, T. & Hauber, M. E. 2008 The
modelling of avian visual perception predicts behavioural
rejection responses to foreign egg colours. Biol. Lett. 4,
515–517. (doi:10.1098/rsbl.2008.0279)
Chiao, C.-C., Chubb, C., Buresch, K. C., Siemann, L. &
Hanlon, R. T. 2009 The scaling effects of substrate tex-
ture on camouflage patterning in cuttlefish. Vis. Res. 49,
1647–1656. (doi:10.1016/j.visres.2009.04.002)
Cohen, J. 1988 Statistical power analysis for the behavioral
sciences. Hillsdale, NJ: Lawrence Earlbaum Associates.
Davies, N. B. 2000 Cuckoos, cowbirds and other cheats.
London, UK: T & A D Poyser.
Davies, N. B. & Brooke, M. de L. 1989 An experimental
study of co-evolution between the cuckoo, Cuculus
canorus, and its hosts. I. Host egg discrimination.
J. Anim. Ecol. 58, 207– 224.
Godfrey, D., Lythgoe, J. N. & Rumball, D. A. 1987 Zebra
stripes and tiger stripes: the spatial frequency distribution
of the pattern compared to that of the background is
significant in display and crypsis. Biol. J. Linn. Soc. 32,
427–433. (doi:10.1111/j.1095-8312.1987.tb00442.x)
Gosler, A. G., Barnett, P. R. & Reynolds, S. J. 2000 Inheri-
tance and variation in eggshell patterning in the great tit,
Parus major.Proc. R. Soc. Lond. B 267, 2469–2473.
(doi:10.1098/rspb.2000.1307)
Hart, N. & Hunt, D. 2007 Avian visual pigments: charac-
teristics, spectral tuning, and evolution. Am. Nat. 169,
7–26.
Hart, N. S., Partridge, J. C., Cuthill, I. C. & Bennett,
A. T. D. 2000 Visual pigments, oil droplets, ocular
media and cone photoreceptor distribution in two species
of passerine: the blue tit (Parus caer uleus L.) and the
blackbird (Turdus merula L.). J. Comp. Physiol. A 186,
375–387. (doi:10.1007/s003590050437)
Jones, C. D. & Osorio, D. 2004 Discrimination of orientated
visual textures by poultry chicks. Vis. Res. 44, 83–89.
(doi:10.1016/j.visres.2003.08.014)
20 40
host rejection rate (%)
number of matching pattern attributes
60 80 100
5brambling
pied
wagtail
garden
warbler
red-
backed
shrike
reed
warbler
meadow
pipit
dunnock
great
reed
warbler
4
3
2
1
0
Figure 2. The relationship between the likelihood that hosts
will reject non-mimetic eggs and the number of matching
pattern attributes. Pattern attributes are marking (filter)
size, proportion energy, total pattern contrast (energy), pat-
tern coverage and pattern dispersion. Rejection rates are
taken from Avile
´s & Garamszegi (2007).
1392 M. C. Stoddard & M. Stevens Pattern mimicry of host eggs by cuckoo
Proc. R. Soc. B (2010)

Lahti, D. & Lahti, A. 2002 How precise is egg discrimination
in weaverbirds? Anim. Behav. 63, 1135 – 1142. (doi:10.
1006/anbe.2002.3009)
Langmore, N. E., Stevens, M., Maurer, G. & Kilner, R. M.
2009 Are dark cuckoo eggs cryptic in host nests? Anim.
Behav. 78, 461– 468. (doi:10.1016/j.anbehav.2009.06.
003)
Lo
´pez-de-Hierro, M. & Moreno-Rueda, G. In press. Egg-
spot pattern rather than egg colour affects conspecific
egg rejection in the house sparrow (Passer domesticus).
Behav. Ecol. Sociobiol. (doi:10.1007/s00265-009-0811-9)
Moksnes, A. & Røskaft, E. 1995 Egg-morphs and host pre-
ference in the common cuckoo (Cuculus canorus): an
analysis of cuckoo and host eggs from European
museum collections. J. Zool. 236, 625– 648. (doi:10.
1111/j.1469-7998.1995.tb02736.x)
Moska
´t, C., Sze
´kely, T., Cuthill, I. & Kisbenedek, T. 2008
Hosts’ responses to parasitic eggs: which cues elicit
hosts’ egg discrimination? Ethology 114, 186–194.
Nakagawa, S. & Cuthill, I. 2007 Effect size, confidence inter-
val and statistical significance: a practical guide for
biologists. Biol. Rev. 82, 591– 605. (doi:10.1111/j.1469-
185X.2007.00027.x)
Nguyen, L. P., Nol, E. & Abraham, K. F. 2007 Using digital
photographs to evaluate the effectiveness of plover egg
crypsis. J. Wild. Manage. 71, 2084–2089. (doi:10.2193/
2006-471)
Osorio, D. & Vorobyev, M. 2005 Photoreceptor spectral sen-
sitivities in terrestrial animals: adaptations for luminance
and colour vision. Proc. R. Soc. B 272, 1745 – 1752.
(doi:10.1098/rspb.2005.3156)
Polac
ˇikova
´, L., Honza, M., Procha
´zka, P., Topercer, J. &
Stokke, B. G. 2007 Colour characteristics of the blunt
egg pole: cues for recognition of parasitic eggs as revealed
by reflectance spectrophotometry. Anim. Behav. 74, 419 –
427. (doi:10.1016/j.anbehav.2006.10.023)
Rothstein, S. I. 1990 A model system for coevolution: avian
brood parasitism. Ann. Rev. Ecol. 21, 481– 508. (doi:10.
1146/annurev.es.21.110190.002405)
Safran, R. J. & Vitousek, M. N. 2008 Evolutionary biology:
arms races in the eye of the beholder. Curr. Biol. 18,
R734–R736. (doi:10.1016/j.cub.2008.07.045)
Sanz, J. J. & Garcı
´a-Navas, V. 2009 Eggshell pigmentation
pattern in relation to breeding performance of blue tits
Cyanistes caeruleus.J. Anim. Ecol. 78, 31– 41. (doi:10.
1111/j.1365-2656.2008.01465.x)
Stevens, M. & Cuthill, I. C. 2006 Disruptive coloration,
crypsis and edge detection in early visual processing.
Proc. R. Soc. B 273, 2141 –2147. (doi:10.1098/rspb.
2006.3556)
Stevens, M., Pa
´rraga, C. A., Cuthill, I. C., Partridge, J. C. &
Troscianko, T. S. 2007 Using digital photography to study
animal coloration. Biol. J. Linn. Soc. 90, 211– 237.
(doi:10.1111/j.1095-8312.2007.00725.x)
Pattern mimicry of host eggs by cuckoo M. C. Stoddard & M. Stevens 1393
Proc. R. Soc. B (2010)