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Abstract

Several antipredator strategies are related to prey colouration. Some colour patterns can create visual illusions during movement (such as motion dazzle), making it difficult for a predator to capture moving prey successfully. Experimental evidence about motion dazzle, however, is still very scarce and comes only from studies using human predators capturing moving prey items in computer games. We tested a motion dazzle effect using for the first time natural predators (wild great tits, Parus major). We used artificial prey items bearing three different colour patterns: uniform brown (control), black with elongated yellow pattern and black with interrupted yellow pattern. The last two resembled colour patterns of the aposematic, polymorphic dart-poison frog Dendrobates tinctorius. We specifically tested whether an elongated colour pattern could create visual illusions when combined with straight movement. Our results, however, do not support this hypothesis. We found no differences in the number of successful attacks towards prey items with different patterns (elongated/interrupted) moving linearly. Nevertheless, both prey types were significantly more difficult to catch compared to the uniform brown prey, indicating that both colour patterns could provide some benefit for a moving individual. Surprisingly, no effect of background (complex vs. plain) was found. This is the first experiment with moving prey showing that some colour patterns can affect avian predators’ ability to capture moving prey, but the mechanisms lowering the capture rate are still poorly understood.
ORIGINAL PAPER
Visual illusions in predator–prey interactions: birds find moving
patterned prey harder to catch
Liisa Ha
¨
ma
¨
la
¨
inen
1
Janne Valkonen
1
Johanna Mappes
1
Bibiana Rojas
1
Received: 16 September 2014 / Revised: 29 April 2015 / Accepted: 29 April 2015
Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Several antipredator strategies are related to
prey colouration. Some colour patterns can create visual
illusions during movement (such as motion dazzle), mak-
ing it difficult for a predator to capture moving prey suc-
cessfully. Experimental evidence about motion dazzle,
however, is still very scarce and comes only from studies
using human predators capturing moving prey items in
computer games. We tested a motion dazzle effect using
for the first time natural predators (wild great tits, Parus
major). We used artificial prey items bearing three different
colour patterns: uniform brown (control), black with
elongated yellow pattern and black with interrupted yellow
pattern. The last two resembled colour patterns of the
aposematic, polymorphic dart-poison frog Dendrobates
tinctorius. We specifically tested whether an elongated
colour pattern could create visual illusions when combined
with straight movement. Our results, however, do not
support this hypothesis. We found no differences in the
number of successful attacks towards prey items with dif-
ferent patterns (elongated/interrupted) moving linearly.
Nevertheless, both prey types were significantly more dif-
ficult to catch compared to the uniform brown prey, indi-
cating that both colour patterns could provide some benefit
for a moving individual. Surprisingly, no effect of back-
ground (complex vs. plain) was found. This is the first
experiment with moving prey showing that some colour
patterns can affect avian predators’ ability to capture
moving prey, but the mechanisms lowering the capture rate
are still poorly understood.
Keywords Aposematism Colour polymorphism
Motion dazzle Predator–prey interactions
Visual illusions
Introduction
Animal colouration has several different functions and the
potential to affect an individual’s fitness significantly (Cott
1940). One important role of colouration is predator
avoidance. Among the various antipredator strategies re-
lated to prey colouration, aposematism and camouflage are
probably the most studied (Poulton 1890; Cott 1940;
Ruxton et al. 2004). Aposem atic species advertise their
unprofitability (e.g. toxicity) with warning signals (Poulton
1890), so that predators learn to avoid them. These signals
are often conspicuous and brightly coloured. Camouflaged
species, on the other hand, rely on colouration that makes
them hard to detect or recognize by predators (Cott 1940),
thereby reducing the chance of bein g attacked. In addition
to these effects, which are thought to work when animals
are still, it has been suggested that colouration could have a
different function when an individual is moving (Thayer
1909; Stevens 2007; Kelley and Kelley 2014). Because
detection by predators is often likely during movement (Sih
1984), it would be beneficial for prey to have colour pat-
terns that hinder capture once detected. Some patterns are
thought to protect moving individuals by creating visual
illusions, effects that may alter the perception of the viewer
(Kelley and Kelley 2014). Such illusions may, for example,
Electronic supplementary material The online version of this
article (doi:10.1007/s10071-015-0874-0) contains supplementary
material, which is available to authorized users.
& Bibiana Rojas
bibiana.rojas@jyu.fi
1
Department of Biological and Environmental Science, Centre
of Excellence in Biological Interactions, University of
Jyva
¨
skyla
¨
, P.O. Box 35, 40014 Jyva
¨
skyla
¨
, Finland
123
Anim Cogn
DOI 10.1007/s10071-015-0874-0
make it difficult for a predator to judge the speed and di-
rection of prey with certain markings (Stevens 2007; Kel-
ley and Kelley 2014), a phenomenon called motion dazzle.
These markings include bars, stripes and zigzag patterns,
which are all common in the animal kingdom (Cott 1940),
indicating that the motion dazzle effect could potentially
work in a variety of species.
Some observational studies have found a correlation
between animal escape behaviour, or type of movement,
and colour patterns (Jackson et al. 1976; Pough 1976;
Brodie 1992; Allen et al. 2013; Rojas et al. 2014). For
example, Jackson et al. (1976) examined the colour pat-
terns and behaviour of several snake species in northern
Mexico and found that those with striped patterns, as well
as uniformly coloured species, were likely to rely on
fleeing as their antipredator strategy. Species with blotched
or spotted patterns, in contrast, rely on the disruptive ele-
ments of their colouration to avoid detection by predators
in the first place. In a more recent study, Allen et al. (2013)
found the same association of longitudin al stripes and rapid
escape speed in Australian and North American snakes.
Jackson et al. (1976) suggested that uniform and striped
patterns are suitable for a rapid escape as a primary defence
because these patterns could generate the illusion of im-
mobility in an individual moving rapidly. They concluded
that this phenomenon occurs because these patterns do not
have any reference points that allow an observer to detect
forward movement (Jackson et al. 1976). Therefore, these
patterns could elevate the threshold velocity for movement
recognition and confuse preda tors. This idea obtained
support when Brodie (1989) found that colour pattern and
antipredator behaviour were genetically correlated in col-
our polymorphic, nonaposematic garter snakes (Thamno-
phis ordinoides). Again, individuals with striped patterns
relied on direct flight, whereas individuals with unmarked,
spotted or broken patterns showed more cryptic behaviour,
changing direction during flight. Both combinations
seemed to increase the survival of individuals (Brodie
1992), and therefore, Brodie suggested that correlational
selection could be the mechanism favouring them.
Although there are several studies about motion dazzle
(e.g. Jackson et al. 1976; Pough 1976; Brodie 1992), most
of them have provided only correlational evidence of an
association between colour patterns and behaviour. All the
experimental studies to date have used games with humans
as predators, trying to catch computer-generated moving
prey with different colour patterns (Stevens et al. 2008,
2011; Scott-Samuel et al. 2011; von Helversen et al. 2013;
Hughes et al. 2014). These studies have provided some
evidence of motion dazzle, showing that high-contrast
patterns (e.g. bands, stripes and zigzag patterns) are more
difficult to capture compared to conspi cuous uniform
colouration (Stevens et al. 2008, 2011). In contrast, von
Helversen et al. (2013) found that longitudinally and ver-
tically striped objects were actually captured more easily
compared to objects with uniform colouration.
Motion dazzle, however, has never been tested ex-
perimentally with any predators other than humans. There
are many between-species differences in visual systems
(Cuthill et al. 2000
; Stevens 2007; Kelley and Kelley
2014), and visual illusions could be perceived in different
ways across species (Nakamura et al. 2006; Pepperber g
et al. 2008; Watanabe et al. 2011, 2013 ). Knowing that
birds are capable of detecting movement and recognize
objects in motion (Dittrich and Lea 2001), we tested for the
first time how avian predators respond to possible visual
illusions by using wild great tits (Parus major). Birds are
an important predator group for many species in different
taxa (e.g. Niskan en and Mappes 2005; Noonan and
Comeault 2009; Nokelainen et al. 2014), and therefore, an
experiment with bird predators may provide relevant in-
formation about how motion dazzle works in nature.
To make the situation more realistic, we used colour
patterns that exist in nature. Previous studies with humans
and computer games (Stevens et al. 2008, 2011; Scott-
Samuel et al. 2011; von Helversen et al. 2013) have all
used simplified black and white patterns, for example,
longitudinal and vertical stripes. However, to avoid any
direct interference from the birds’ previous experience, we
chose patterns that came from an organism they could not
have encountered before, the aposematic poison frog
Dendrobates tinctorius (Fig. 1). Dendrobates tinctorius has
yellow and black dorsal colour patterns that vary sig-
nificantly within (Rojas and Endler 2013) and among
populations (Wollenberg et al. 2008). It is diurnal and field
experiments with plasticine models suggest that it may
suffer attacks from birds (Noonan and Comeault 2009). In
a previous study, Rojas et al. (2014) found a connection
between colour pattern geometry and movement type of
Fig. 1 Typical colour patterns of Dendrobates tinctorius: an indi-
vidual with an interrupted yellow pattern (a) and an individual with an
elongated yellow pattern (b)
Anim Cogn
123
frog individuals. Individuals with more elongated colour
patterns showed directional movement with higher linear
speed, over longer segments in their trajectories, compared
to individuals with more interruptions in their y ellow
patches, which changed direction unpredictably and moved
at lower linear speed and over shorter segments.
Rojas et al. (2014) suggested that the observed combi-
nations of certain colour patterns and behaviours could
benefit individuals by making them less vulnerable to
predation. They propose that individuals with more elon-
gated yellow patterns (Fig. 1b) could benefit from direc-
tional and fast movement because this combination could
create the illusion of immobility or reduced speed. Frogs
with interrupted patterns (Fig. 1a), on the other hand,
would benefit from rando m and slow movement, given that
interrupted patterns could be visually disruptive (Cott
1940; Stevens 2007), and together with a slower movement
could help to avoid motion-oriented predators (Hatle and
Faragher 1998; Hatle et al. 2002). Thus, different colour
patterns of D. tinctorius could be efficient against preda tors
when combined with a specific type of movement (Rojas
et al. 2014), and this might enabl e different colour morphs
to remain in the same population.
The field study by Rojas et al. (2014), however, pro-
vided only correlational evidence and did not look at
predator response to these colour patterns and movement
combinations. The aim of our study was to test ex-
perimentally how these combinations work against avian
predators. We used great tits, which have been used as a
model for bird perception of signals for decades, as
predators. Notably, these birds are naı
¨
ve to the patterns
used, which was essential for our experiment. Therefore,
possible differences in the capture success betwee n dif-
ferent prey patterns should be detected. It is important to
clarify that the purpose of our experiment was not to study
how easily great tits would prey on dyeing poison frogs.
Specifically, our aim was to determ ine whether linearly
moving prey with elongated colour p atterns is more diffi-
cult to catch by predators than prey with interrupted or
uniform colour patterns. We tested this by placing a great
tit in an experimental cage and moving prey items bearing
different patterns (uniform brown, elongated and inter-
rupted) linearly across the cage floor, recording the number
of successful attacks. Our hypothesis was that prey with an
elongated pattern would experience the least number of
successful attacks because this pattern could create a mo-
tion dazzle effect, making it more difficult for birds to
direct their attack. If so, individuals with more elongated
patterns would benefit from moving directionally, which
could help explaining the differences in the behaviour of
frog individuals observed in the field (Rojas et al. 2014). In
addition, we also used two different backgrounds: plain and
leaf litter, and hypothesized that prey items would be more
difficult to capture in a more com plex background.
Therefore, we predicted a lower number of successful at-
tacks with a leaf-litter background.
Materials and methods
Predators
We used wild-caught great tits as predators. Birds were
caught from a feeding site and kept in captivity for ap-
proximately 5 days. They were housed individually in
plywood cages with a daily light period of 11 h, fed on
sunflower seeds, peanuts and tallow, and provided with
fresh water ad libitum. The sex and age of each individual
were recorded, and after the experiment, all birds were
ringed for identification purposes before being released at
the capture site. Altogether, we used 30 birds (15 males, 15
females).
The experiment was conducted at Konnevesi Research
Station in Central Finland from October to December 2013.
Wild birds were used with permission from the Central
Finland Centre for Economic Development, Transport and
Environment and licence from the National Animal Ex-
periment Board, and used according to the ASAB guide-
lines for the treatment of animals in behavioural research
and teaching.
Prey items and experimental cage
Artificial prey items consisted of two 17-mm-long, oval-
shaped pieces of paper, glued together and holding a small
piece of mealworm (Tenebrio molitor) in the middle. Each
prey item had one of three possible colour patterns (shown
in Fig. 2): a uniform brown (control), and two other re-
sembling colour patterns of D. tinctorius, an elongated
pattern and an interrupted one. The brown prey item was
chosen as a control in order to compare the attack success
between conspicuous frog patterns and camouflaged, uni-
coloured prey items. The same colour tones were used for
the yellow and black of the p atterned prey, so that both of
them were equally different from the brown control prey,
regardless of their colour distribution in the great tit’s te-
trahedral vision space.
The experiment was conducted in a 76 9 60 9 77 cm
size plywood cage. The cage was illuminated with a light
bulb, and it had two perches at a height of 64 cm. Birds
were observed through a one-way glass in the front wall.
Prey items moved in a straight line across the cage using a
motor-driven belt that circulated under the cage floor. A
screw was attached to the belt, and a 5-mm-wide slit on the
cage flo or allowed the screw to move from one side of the
cage to the opposite. In that way, birds were able to see the
Anim Cogn
123
prey items only while the screw they were attached to
moved linearly across the cage floor.
We did the experiment with two different backgrounds.
The light brown floor of the cage was used as a plain
background, whereas the other background resembled leaf
litter, which is the natural background of D. tinctorius.This
was done by taping coloured leaf-litter patterned sheets of
paper on the cage floor (Fig. 2).
Bird training
Before the exper iment, birds were trained in their home
cages to consume artificial prey items that were still. This
was done in order to familiarize the birds with the different
colour patterns to be used in the experiment, and to moti-
vate them to attack these prey when moving. The purpose
of the training was also to make sure that birds associated
all prey patterns with palatable food, so that after the
training, they did not have biases towards any of the prey
items. This was important because we wanted to test the
capture succe ss and any hesitation to attack could have
lowered the capture rate and affected the results.
In order to identify a possible innate preference or
aversion towards any of the patterns, we recorded the order
in which 10 birds ate the different prey items during the
training. This was done by offering each bird all three prey
items (uniform brown, elongated and interrupted) at the
same time, and recording both the order in which birds ate
them and the time until they started to eat. For every bird,
this was repeated five times so that every bird ate 15 prey
items altogether (five of each prey type) during the pref-
erence test. The 20 birds that were not used in this pref-
erence test were equally trained with 15 prey items.
Therefore, all birds used in the actual experiment had the
same training, which would ensure the association of the
three patterns with a (palatable) reward.
Once birds were familiarized with prey items, one bird
at a time was placed in the experimental cage. We waited
for birds to habituate to the cage and let the motor run
without prey items so that the birds also got used to the
noise. Birds were trained to attack moving prey items by
offering them a piece of mealworm moving slowly across
the cage. Each bird was presented at least four slow-
moving mealworm pieces. If the bird kept hesitating to
attack after those four trials, more training was done. After
the training, birds were food-deprived for 45 min to ensure
their motivation to attack during the experiment.
Experimental design
We tested 15 birds with a plain background, and the other
15 with a leaf-litter background. Birds were assigned to
each background treatment randomly, but we checked that
there were no biases in age or sex between the two groups.
All birds were trained with the actual background they had
during the experiment.
The experiment consisted of five trials in each of which
birds were pres ented with all three different prey types in a
randomized order. Prey moved across the cage with a speed
of 16 cm/s. This speed was chosen based on preliminary
observations, so that it was n ot too easy for the birds but
also not unrealistically high. The direction of the move-
ment was changed randomly between different prey items,
such that sometimes prey came from the left side of the
cage and sometimes from the right side.
We let the prey item run across the cage until the bird
attacked. Birds were considered to attack when they clearly
tried to peck the moving prey item. If the attack was suc-
cessful, we let the bird eat the prey, but if the bird did not
manage to catch the prey item in the first attempt, we
stopped the motor and replaced it with the next prey type.
So, if the bird did not attac k the prey within the first 20
rounds (i.e. belt cycles), we gave it a 10-min break (waiting
for the bird to be more motivated), after which the same
prey item was offered again, continuing for as long as it
took for the bird to attack. In many instances, the birds
approached the prey but did not try to hit it. However, we
Fig. 2 Three different patterns used during the experiments, striped
(left); interrupted (middle); and uniform (right), against (a) leaf litter
and (b) plain background
Anim Cogn
123
did not count that as an attack and waited until the bird
actually tried to hit the prey item. This means that all the
unsuccessful attacks were truly unsuccessful, and there
were thus no ‘unrealized’ attacks.
In the course of each trial, we had a 3-min break be-
tween different prey items (i.e. after each attack). During
these 3 min, we let the motor run before offering the next
prey, but stopp ed it a few times at random intervals to
prevent the birds from associating these pauses with the
appearance of food. We also had a 10-min break between
the trials to make sure that the bird was motivated to attack.
During the breaks, we let the motor run witho ut prey items
so that the birds did not associate the motor sound with
food. All trials were recorded with a video camera (Canon
Legria HF R37).
During the experiment, we counted the number of
rounds it took for a bird to attack each prey item and
classified each attack as successful (a bird captured the
prey item) or unsuccessful (a bird attacked but did not
capture the prey item). Afterwards, we measured from the
videos how long it took for a bird to start the attack after
the prey item was exposed. We also checked whether the
attack was unsuccessful because birds failed to hit the prey,
or because they did not manage to detach it from the screw.
Statistical analyses
We used a generalized linear mixed model (GLMM) with
binomial error distribution to analyse the differences in the
number of successful attacks between different prey types.
We used the success of attack (0/1) as a binary response
variable, and pattern (elongated/interrupted/control), trial
number (1–5), background (plain/litter) and order (the
order in which prey items were presented to a bird within a
trial) as explanatory variables. In addition, we used bird
identity (ID) as a random factor in the model. We started
the model selection with the model that included also sex
and age of the bird and interactions between pattern and
trial and pattern and background. However, these terms
were nonsignificant, and dropping them out from the model
did not reduce the fit of our model significantly (Table 1).
The differences in the time before birds started their
attack were analysed using a mixed-effects Cox model. The
time before attack started was used as response variable
and pattern, trial number, background, order and attack
success were explanatory variables. Again, bird ID was
entered as a random factor. Interactions between pattern
and background, and pattern and trial were included in the
first model, but interaction between pattern and trial was
removed from the final model because it did not change
model fit significantly (Table 2).
A mixed-effects Cox model was used also to test for
possible avoidance or preference towards the different prey
types during the training session (i.e. before the actual
experiment). The order in which prey items were consumed
was used as a response variable, pattern as an explanatory
variable and bird ID as a random factor. The differences in
time before birds ate prey items during the training were
analysed simi larly, using now time before eating as a re-
sponse variable. All statistical analyses were done with the
software R 3.0.2, using packages lme4 and coxme.
Table 1 Comparisons of GLMMs explaining attack success on prey
items
Model Model df AIC v
2
df P
a 22 496.58
b 14 487.03 0.124 8 0.597
c 12 487.73 4.701 2 0.095
d 11 485.86 6.448 1 0.725
Model a included explanatory variables pattern ? background
? trial ? order ? sex ? pattern:background; model b, pattern ?
background ? trial ? order ? sex ? pattern:background; model c,
pattern ? background ? trial ? order ? sex; and model d, pat-
tern ? background ? trial ? order. Bird ID was included as a ran-
dom factor in each model
Table 2 Mixed-effects Cox model explaining the time before birds
started their attack in the experiment
Source Coefficient ZP
Interrupted -0.3735 -1.39 0.160
Striped 0.0348 0.13 0.900
Plain background -0.0236 -0.17 0.860
Trial 2 -0.3241 -1.21 0.230
Trial 3 -0.1215 -0.45 0.650
Trial 4 -0.10119 -0.38 0.710
Trial 5 -0.2908 -1.07 0.290
Order 2 -0.077 -0.64 0.520
Order 3 0.0909 0.75 0.450
Successful attack 0.1949 1.63 0.100
Interrupted: trial 2 0.6770 1.79 0.074
Striped: trial 2 0.2171 0.58 0.560
Interrupted: trial 3 0.3161 0.84 0.400
Striped: trial 3 0.0773 0.21 0.840
Interrupted: trial 4 0.3065 0.81 0.420
Striped: trial 4 -0.0148 -0.04 0.970
Interrupted: trial 5 0.5626 1.48 0.140
Striped: trial 5 0.4491 1.19 0.230
Time before attack is used as a response variable. Prey pattern,
background type, trial number, order in which prey items were pre-
sented to birds within a trial, attack success and interaction between
prey pattern type and trial were fixed factors, and bird ID a random
factor. The reference level is the control pattern with leaf-litter
background in the first trial, when control prey item is the first one to
be presented within this trial (order 1) and attack is unsuccessful
Anim Cogn
123
Results
Overall, birds captured 66 % of the moving prey items
successfully. In most of the cases, the unsuccessful attacks
were directed behind the prey, i.e. birds jumped behind the
prey trying to hit it but were unable to reach it (see sup-
plementary material for videos of a successful and an un-
successful attack). Control (uniform brown) prey items
were captured significantly more often than elongated and
interrupted ones (Table 3; Fig. 3). There was no significant
difference in the success of attack between elongated and
interrupted prey (estimate =-0.002, Z =-0.007,
P = 0.994). For all patterns, the percentage of successful
attacks was higher in the last trials (Table 1), show ing the
clear learning curves during the experiment (Fig. 4). The
background and the order in which prey items were pre-
sented within a trial did not have a significant effect on the
success of attack (Table 3).
The time before birds started their attack did not differ
significantly between prey items with elongated and in-
terrupted patterns (coefficient = 0.37, Z = 1.53,
P = 0.13) or between control prey items and either of these
patterns (Table 4). Also, background, trial number, order in
which prey items were presented within a trial or the
success of attack did not have a significant effect on the
time before birds started the attack (Table 4).
During training, the birds did not seem to avoid or prefer
either elongated pattern (Z =-1.12, P = 0.26) or inter-
rupted pattern (Z =-1.00, P = 0.32) compared to the
control. Also, there were no differences in the preferences
between these two different patterns (Z =-0.13,
P = 0.90). Similarly, the time before birds ate the prey
items during training did not differ between control and
elongated ( Z = 0.75, P = 0.46), control and interrupted
(Z =-0.04, P = 0.97) or elongated and interrupted
(Z = 0.71, P = 0.48) prey items, suggesting no pre- exist-
ing biases in favour or against any of the patterns consid-
ered in the study.
Table 3 GLMM explaining the attack success in the experiment
Source Estimate ZP
Intercept -0.2985 -0.652 0.5143
Interrupted -0.8498 -2.815 0.0049
Elongated -0.8517 -2.822 0.0048
Plain background 0.7775 1.651 0.0988
Trial 2 0.5264 1.535 0.1247
Trial 3 1.6446 4.472 \0.0001
Trial 4 1.8701 4.955 \0.0001
Trial 5 2.8971 6.480 \0.0001
Order 2 -0.0883 -0.302 0.7624
Order 3 0.2693 0.915 0.3602
Attack success was included as a response variable and prey pattern,
background type, trial number and order in which prey items were
presented to birds within a trial were fixed factors. In addition, bird ID
was included in the model as a random factor. Intercept gives the
estimate for the control pattern with leaf-litter background in the first
trial, when prey item is the first one to be presented within this trial
(order 1)
Fig. 3 Overall attack success and its 95 % confidence interval for
different prey types: uniform (left), striped (middle) and interrupted
(right)
Fig. 4 Attack success in different trials during the experiment. The
solid line represents the learning curve for uniformly coloured
(brown) prey. The dotted lines (yellow and blue) represent the
learning curve for prey items with striped and interrupted patterns.
These two curves overlap because of undistinguishable differences in
bird response (colour figure online)
Anim Cogn
123
Discussion
Our study shows that some colour patterns can benefit
moving prey by lower ing the rate of successful attacks. We
found that it was easier for birds to capture a uniformly
coloured prey item compared to prey with striped or in-
terrupted yellow colour patter ns. However, in contrast to
our predictions, there was no difference in the capture rate
between these two different pattern types.
This is the first time that a motion dazzle effect has been
tested with avian predators. Previous studies with human
predators and computer-generated prey items have shown
that although a camouflaged grey item was most difficult to
capture, different high-contrast patterns (e.g. bands, stripes
and zigzag patterns) also lowered the capture rate com-
pared to uniform conspi cuous colouration (Stevens et al.
2008, 2011). This is consistent with our results that also
found uniformly coloured prey items to be easiest to cap-
ture, even though the unicoloured prey items in our ex-
periment were not conspicuous. On the other hand, a recent
study showed opposite results, finding that human preda-
tors captured longitudinally and vertically striped objects
more often than objects with uniform colouration (von
Helversen et al. 2013). The authors suggest that this result
might be explained by how the prey in their experiment
was captured by the predators (humans, in this case).
Participants were asked to ‘attack’ only once the prey had
reached a specific zone of the screen, as opposed to a
natural situation where predators would chase the prey,
finding it difficult to hit it due to their dazzle patterns. The
differences between the studies using human predators,
thus, could arise from different experimental designs, but
also from differences between the visual systems of hu-
mans and birds (Nakamura et al. 2006 ). Birds may have,
for example, higher temporal and spatial acuity (Jarvis
et al. 2002). Therefore, experiments with birds are needed
when testing the effect of the colouration of moving prey
against avian predators.
We did not find any difference in the attack success
towards striped versus interrupted colour patterns.
Although birds have shown to be able to recognise dif-
ferent objects in motion (Dittrich and Lea 2001) and to
discriminate among prey with similar patterns (Dittrich
et al. 1993; Green et al. 1999), it has been suggested that
predators find difficult to follow the movement of prey with
striped patterns (Jackson et al. 1976). This is most likely
because striped patterns in motion do not have any refer-
ence points on which a predator could focus. Thus, we
expected birds to find prey with elongated patterns more
difficult to capture; our results, however, do not support
this motion dazzle hypothesis. Instead, both interrupted and
striped patterns were captured less, suggesting that any
kind of nonuniform pattern could protect an individual
from predators during movement. Our experiment, though,
does not reveal the mechanisms that made these patterns
more difficult to capture. About half of the times, the attack
was unsuccessful because birds failed to hit the moving
prey object, which may indicate diffi culties in the accurate
estimation of speed. There is some evidence (Scott-Samuel
et al. 2011; von Helversen et al. 2013) that targets with
patterns could be perceived to move either faster or slower
compared to plain objects, which could make it more dif-
ficult to hit them. Scott-Samuel et al. (2011) showed that
objects with zigzag or check patterns were perceived to
move slower than objects with plain patterns, although this
difference was found only when patterns had a high con-
trast against their background and objects were movi ng at
high speed. In contrast, von Helversen et al. (2013) found
that longit udinally and vertically striped objects were ac-
tually perceived to move faster than unicoloured obje cts.
These studies, however, presented prey with repeated pat-
terns (bars, stripes, etc.) on computer screens, which was
not the case in our study.
On several occasions, birds hit the moving prey item,
but the attack was unsuccessful because they did not
manage to detach it from the screw to where it was at-
tached. This could mean that the pattern made it more
difficult for the bird to p erceive the shape of the prey object
and thus direct the attack and grab it successfully, i.e. the
object may have benefited from a disruptive effect (Stevens
and Merilaita 2009). Of course, it is also possible that prey
colouration (uniform brown vs. black and yellow patterns)
could cause the observed differences in the attack success.
The two colour patterns used in our experiment both re-
sembled aposematic frogs, which could evoke in the birds
an innate hesitation to grab them. However, birds never had
a chance to associate these patterns with anything un-
palatable, and even though they might have some innate
aversion to these colour combina tions (Schuler and Hesse
1985; Lindstro
¨
m et al. 1999), they had been trained to
associate the three types of prey with a palatable reward.
Moreover, the preference test during the training showed
that birds did not seem to avoid or prefer any of the prey
Table 4 Comparisons of mixed-effects Cox models explaining delay
before the birds started their attacks on prey items
Model Model df AIC
v
2
df P
a21 -15.66
b19 -17.04 5.379 2 0.068
c11 -6.11 5.074 8 0.750
Model a included explanatory variables pattern ? background ?
trial ? order ? success ? pattern:background ? trial:pattern; model
b, pattern ? background ? trial ? order ? success ? trial:pattern;
and model c, pattern ? background ? trial ? order ? success. Bird
ID vas includes as a random factor in each model
Anim Cogn
123
types. Furthermore, the time before birds started their at-
tack did not differ between prey objects, indicati ng that
birds did not hesitate more to attack prey with warning
signals. Thus, aposematism does not seem to explain the
observed differences in the attack success.
Surprisingly, the backgr ound did not affect the attac k
success or the time delay before birds started their attac k.
We predicted that the more complex leaf-litter background
would have made prey capture more difficult. This was
found in a computer game experiment (Stevens et al.
2008), which showed that human predators missed more
prey items when the background was more heterogeneous.
In addition, it has been shown that background can affect
the perceived speed of a target (Blakemore and Snowden
2000). However, birds in our experiment seemed to capture
prey items equally well in both backgrounds. It is possible
that yellow warning signals made patterned prey items easy
to detect even on a more heterogeneous background. On
the other hand, the leaf-litter background did not provide
better concealment even for the uniform brown prey items,
so it seems that movement made all prey items easily de-
tectable regardless of the background.
Birds learned to capture prey items better throughout the
experiment, and the success of attack increased towards the
last trials. Many previous studies have shown that great tits
are able to learn relatively complex tasks (e.g. Lyytinen
et al. 2004), so the improvement in attack success with time
was not surprising. There were clear learning curves for all
prey types (Fig. 4), showing that experienced birds cap-
tured also both patterns more easily in the last trials. This
suggests that colour patterns could be most effective
against naı
¨
ve predators and that predators might be able to
improve their capture success with experience. On the
other hand, our study design was simplified compared to
real situations in nature. Although we changed the direction
of the movement randomly, such that sometimes prey items
were moving from right to left and sometimes from left to
right, prey was always crossing the front part of the cage,
moving in a straight line and at constant speed. This
probably made it easy for the birds to learn to predict prey
movement and increase their capture rate. In more realistic
situations, prey trajectory would not be that predictable.
Also, when moving through the vegetation, prey might not
be clearly visible all the time, making it more difficult for a
predator to follow them.
In our experiment, prey items moved at a speed of
16 cm/s, but it is not known how high speed must be for
visual illusions to occur. It is possible that prey movement
was not fast enough to cause a motion dazzle effect, and
this could explain why there were no differences in the
attack success between elongated and interrupted patterns.
In an experiment with humans (Stevens et al. 2008), all
prey items were harder to catch at fast (20 cm/s) than at
slow speed (15 cm/s), but there was no interaction betwee n
the speed and the prey type. This means that same prey
types were most difficult to capture in both speeds, and
thus, the occurrence of motion dazzle did not seem to de-
pend on the speed. When considering D. tinctorius indi-
viduals, the speed that we used was probably in the upper
limit of their moving ability and higher speed may not be
realistic for the frogs. The previous field study with the
species (Rojas et al. 2014) showed that frogs with elon-
gated patterns moved direct ionally, at a speed of 1.14 cm/s,
whereas frogs with more interrupted patterns moved
slower, 0.31 cm/s. However, these are only the average
speeds over each segment, including brief pauses during
movement, so the maximum speed of the frogs is higher.
Moreover, frogs can do long jumps when escaping preda-
tors, and it is this fast movement that could potentially
cause visual illusions and confuse predators. Therefore,
instead of considering only the average linear speed, also
the speed of movement bursts should be taken into account
when studying motion dazzle in animals (Rojas et al.
2014).
We did not find any evidence that prey with striped
patterns benefitted more from the linear movement com-
pared to prey with more interrupted patterns; hence, the
hypothesis that visual illusions could explain the observed
connection between colour pattern and movement type in
D. tinctorius was not supported. Rojas et al. (2014) sug-
gested that motion dazzle could be one possible explanation
for linear movement to be advantageous for individuals
with more elongated patterns. However, our study did not
provide any evidence that the fitness of frog individuals
would depend on the combination of their movement and
colour pattern. Instead, the results of our experiment sug-
gest that both elongated and interrupted colour patterns are
equally difficult to capture, and in that sense, the fitness of
both colour morphs is the same. This may allow both of
them to coexist in the same population, but does not explain
the observed differences in their movement.
Overall, our study provided the first experimental evi-
dence that colour patterns can affect the ability of birds to
capture moving prey items. All previous studies have used
human predators, but becau se visual processing is different
between different species (Stevens 2007 ; Kelley and Kel-
ley 2014), it is important to get information on how other
predators perceive visual illusions. Our results showed that
patterned prey, regardless of the pattern type, is more dif-
ficult to catch compared to prey with uniform colouration.
This supports the idea that instead of some specific mark-
ings, many different patterns have the potential create vi-
sual illusions. There are still relatively few studies that
have investigated the function of colour patterns during
movement and theref ore this provides a promising area for
further research.
Anim Cogn
123
Acknowledgments We are most grateful to Helina
¨
Nisu for taking
care of the birds, to Morgan Brain for help during the preference tests,
and to Laura Kelley for helpful comments on the manuscript. Permits
for experiments with wild birds were issued by the Central Finland
Centre for Economic Development, Transport and Environment
(KESELY/1017/07.01/2010) and the National Animal Experiment
Board (ESAVI-2010-087517Ym-23). The study was funded by So-
cietas Biologica Fennica Vanamo (grant to LH), and the Finnish
Centre of Excellence in Biological Interactions (project SA-252411).
Conflict of interest None.
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