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Variation in predator behavior toward aposematic prey was frequently studied at interspecific and individual levels, but interpopulation differences have been neglected. Geographic differences in prey fauna offer an opportunity to test their implications for predator behavior. It can be expected that 1) predator populations inhabiting environments with high diversity of aposematic prey are more neophobic than those living in areas where aposematic prey are scarce, and 2) different levels of neophobia jointly with avoidance learning affect selection on aposematic prey. We compared the behavior of wild-caught great tits (Parus major) from Bohemia and Central Finland toward aposematic firebugs (Pyrrhocoris apterus), nonaposematic firebugs, novel objects and novel palatable nonaposematic prey. Finnish and Bohemian birds did not differ in their novel-object exploration, but Finnish birds hesitated longer than Bohemian birds before resuming feeding next to a novel object. Latencies to attack novel palatable prey did not differ and were not correlated with the attitude toward novel objects. Tits from the Bohemian population mostly avoided aposematic firebugs and attacked nonaposematic ones. Finnish birds were more likely to attack both firebug color forms, and their attack latencies were correlated with latencies of attacking novel palatable prey. Thus, Bohemian birds avoided the aposematic prey, but were not more neophobic than Finnish birds. These results suggest that differences between Finnish and Bohemian birds in behavior to aposematic prey do not follow differences in exploration strategy and neophobia. The observed differences can be explained by a different experience with local aposematic prey communities.
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Original Article
Dierent reactions to aposematic prey in
2 geographically distant populations of
and JohannaMappes
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 43 Praha
2, Czech Republic and
University of Jyvaskyla, Centre of Excellence in Biological Interactions,
Department of Biological and Environmental Science, PO Box 35, Jyväskylä 40014, Finland
Received 26 August 2014; revised 27 May 2015; accepted 30 May 2015.
Variation in predator behavior toward aposematic prey was frequently studied at interspecific and individual levels, but interpopula-
tion differences have been neglected. Geographic differences in prey fauna offer an opportunity to test their implications for predator
behavior. It can be expected that 1)predator populations inhabiting environments with high diversity of aposematic prey are more neo-
phobic than those living in areas where aposematic prey are scarce, and 2)different levels of neophobia jointly with avoidance learn-
ing affect selection on aposematic prey. We compared the behavior of wild-caught great tits (Parus major) from Bohemia and Central
Finland toward aposematic firebugs (Pyrrhocoris apterus), nonaposematic firebugs, novel objects and novel palatable nonaposematic
prey. Finnish and Bohemian birds did not differ in their novel-object exploration, but Finnish birds hesitated longer than Bohemian birds
before resuming feeding next to a novel object. Latencies to attack novel palatable prey did not differ and were not correlated with
the attitude toward novel objects. Tits from the Bohemian population mostly avoided aposematic firebugs and attacked nonaposematic
ones. Finnish birds were more likely to attack both firebug color forms, and their attack latencies were correlated with latencies of
attacking novel palatable prey. Thus, Bohemian birds avoided the aposematic prey, but were not more neophobic than Finnish birds.
These results suggest that differences between Finnish and Bohemian birds in behavior to aposematic prey do not follow differences
in exploration strategy and neophobia. The observed differences can be explained by a different experience with local aposematic
prey communities.
Key words: aposematism, exploration, geographic differences, neophobia, Parus major, Pyrrhocoris apterus.
Avoidance of aposematic prey usually involves several cogni-
tive mechanisms that aect the behavior of predators (Ruxton
etal. 2004). Reaction toward prey may be influenced by neopho-
bia (e.g., Coppinger 1969, 1970; Exnerová etal. 2010) or dietary
conservatism (Marples etal. 1998; Marples and Kelly 1999), and
by inherited (Smith 1975; Lindström et al. 1999a) or learned
(e.g., Lindström etal. 1999b; Exnerová etal. 2007; Aronsson and
Gamberale-Stille 2008; Barnett etal. 2012) aversions against cer-
tain warning signals and their combinations (Marples and Roper
1996; Rowe and Guilford 1996; Lindström et al. 2001). The
response of a predator to warning signals is aected by associa-
tive learning, the degree of which is influenced by memorability,
prey recognition, discrimination, and generalization (Roper and
Redston 1987; Gamberale-Stille and Tullberg 1999; Speed 2000;
Ham et al. 2006; Svádová et al. 2009). Given the complexity of
the cognitive processes, which contribute to the formation of the
avoidance of aposematic prey, it is not surprising that there exists a
considerable variation in behavior of dierent predators toward a
defended prey species (Brower 1988; Exnerová etal. 2003; Endler
and Mappes 2004; Valkonen etal. 2012; Nokelainen etal. 2014).
Predators from dierent taxa may react dierently to a particu-
lar prey species, and several mechanisms have been discussed as
potential factors responsible for the variation: the energetic require-
ments of a predator (i.e., body size or hunger level) are important
in determining whether or not the predator decides to attack and
consume a defended prey (Exnerová etal. 2003; Barnett etal. 2007;
Halpin etal. 2014). Also, sensory and cognitive abilities of preda-
tors can be highly variable (Hart 2001; Sol etal. 2005) influencing
Address correspondence to A.Exnerová. E-mail:
Behavioral Ecology (2015), 00(00), 1–10. doi:10.1093/beheco/arv086
Behavioral Ecology Advance Access published June 25, 2015
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Behavioral Ecology
their ability to learn to avoid aposematic prey (Endler and Mappes
2004). Closely related species also frequently dier in their reac-
tions to novel environments, objects and food; the neophobia level
may be correlated with the degree of habitat and foraging spe-
cialization (Greenberg 1989; Mettke-Hofmann et al. 2009, 2012;
Tebbich etal. 2009).
Variation in reactions to aposematic prey also exists among con-
specific predators, where the initial wariness and rate of avoidance
learning may be correlated with personality traits (Exnerová etal.
2010). On the other hand, the rate of incorporation of a novel food
item into an individual’s diet represents another process: dietary
conservatism (Marples etal. 1998; Marples and Kelly 1999), which
is independent of personality and not correlated with neophobia
(Marples and Mappes 2011). The behavior of predators toward
aposematic prey may also be correlated with their age (Lindström
etal. 1999a; Exnerová etal. 2006; Langham 2006; Mappes etal.
2014), and due to the importance of learning also highly aected
by individual experience (Exnerová et al. 2007; Ihalainen et al.
2008; Barnett etal. 2012; Hotová Svádová etal. 2013).
In contrast to interspecific and individual dierences in behav-
ior toward aposematic prey, the potential dierences between con-
specific populations, namely those living in geographically distant
areas and dierent habitats, have not been studied. Despite being
interesting per se, the knowledge of potential geographical dier-
ences may be important for the generalization of results based on
studies of dierent populations of a particular species of predator.
Individuals from geographically distant populations may react dif-
ferently to aposematic prey simply because of dierent individual
experience with local aposematic prey. Alternatively, the behavior
toward aposematic prey may reflect population-specific dierences
in neophobia (see Liebl and Martin 2014) and exploration strat-
egies evolved for living in dierent conditions such as prey diver-
sity and frequency of noxious prey. Individuals from populations
living in dierent conditions (e.g., dierent predation pressure and
environment stability) dier in their exploration of a novel environ-
ment, and their reactions to novel objects and novel food (Martin
and Fitzgerald 2005; Brydges etal. 2008; Echeverría and Vassallo
2008; Korsten etal. 2010; Liebl and Martin 2014). Likewise, indi-
viduals from migratory populations may be more neophobic than
their resident conspecifics (Mettke-Hofmann etal. 2013).
In this study, we investigated geographical dierences in response
to novel stimuli and reaction to aposematic prey in the great tit
(Parus major L., 1758), a small passerine which is mainly insectivo-
rous during spring and summer, although in autumn and winter,
when insect prey become scarcer, adds berries and seeds to its
diet (Cramp and Perrins 1993). The great tit is a resident species
inhabiting a wide range of woodland habitats in the Palaearctic
region, and its distribution covers the whole Europe including the
far North (Cramp and Perrins 1993). In recent years, the great tit
has become a model species in studies on aposematism and mim-
icry. Because such studies are based on experiments with birds
from various localities across Europe (e.g., Sillén-Tullberg 1985;
Lindström etal. 1999a, 1999b; Exnerová etal. 2006), it is worth
testing whether birds from dierent populations behave in the same
way. As a model aposematic prey we used the firebug (Pyrrhocoris
apterus), which is conspicuously red-and-black colored and unpalat-
able for small passerine birds (Exnerová etal. 2003). The firebug is
widespread in the Palaearctic, but it is absent in Britain and most
of Northern Europe.
By comparing the behavior of wild-caught great tits from 2 geo-
graphically distant areas, Bohemia and Central Finland, we tested
the following hypotheses concerning the reaction of these birds
toward aposematic prey: 1) Dierences in behavior toward apo-
sematic firebugs follow dierences between the 2 populations in
their behavior toward novel palatable prey and other types of novel
objects, that is, they reflect the levels of individual exploration and
neophobia. 2) The 2 populations exhibit specific dierences con-
cerning the aposematic firebugs. The Finnish birds are expected
to be more willing to attack aposematic firebugs because of their
lack of experience with this type of the aposematic prey in their
natural environment. 3)Birds from both populations avoid attack-
ing firebugs regardless of their experience. This may happen if
the avoidance of aposematic prey has a strong genetic basis or the
avoidance learning of prey with a given warning signal is general-
ized to other prey whose signal is similar enough. Because the local
diversity of aposematic prey is important for the interpretation of
the behavior of birds, we also analyzed data on the distribution of
aposematic and nonaposematic species of Heteroptera between the
2 compared areas.
Experiments were carried out at Konnevesi Research Station,
University of Jyväskylä (Central Finland) and in Prague at the
Faculty of Science, Charles University (Bohemia) during autumn
2012. In order to standardize the phenological dierences between
the 2 localities, the experiments were conducted during October in
Central Finland and during November in Bohemia.
Comparison of occurrence of aposematic species
of Heteroptera in Central Europe and Central
In order to compare the composition of the fauna of true bugs
from both areas, we gathered data on the occurrence of heteropter-
ans, particularly of the aposematic species, in Central Europe and
Central Finland. Data for Central Europe were obtained combin-
ing the whole heteropteran faunas of Germany (species included
in Wachmann etal. 2004, 2006, 2007, 2008) and Czech Republic
(Štys P, unpublished data). As for Central Finland, we covered spe-
cies occurring in Finland at the latitude of Konnevesi (62°38N),
or likely to occur there (known to occur slightly more to the South
or to the North), as shown by distributional maps (Rintala and
Rinne 2010). Purely coastal species were excluded. Taxonomically,
we considered only the terrestrial Heteroptera (Leptopodomorpha,
Cimicomorpha, and Pentatomomorpha s. lat.). In their adult stage,
the dorsum of those species regarded as aposematic is uniformly
colored with bright white, yellow, orange or red, or with a combina-
tion of any of those and a contrasting dark pattern. For the pur-
pose of this analysis, we also classified as aposematic those species
having nonaposematic morphs as well. The dull whitish, yellowish
to reddish taxa/morphs were not taken as aposematic (e.g., some
Miridae: Phylinae). All terrestrial true bugs are known to have a
chemical defense (Schuh and Slater 1995).
Altogether we tested 100 wild-caught great tits, 50 from each of 2
geographically distant populations: 1)Konnevesi in Central Finland
(62°38N, 26°19E) and 2) Prague in Bohemia (Czech Republic,
50°04N, 14°26E). The words “Finnish” and “Finland,” when-
ever used without qualification in the text, always refer to Central
Finland at about Konnevesi latitude. The sex and age of both
experimental groups were balanced (Central Finland: 30 males and
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Exneroetal. • Geographic dierences in behavior toward aposematicprey
20 females, 19yearlings and 31 adults; Bohemia: 29 males and 21
females, 17 yearlings and 33 adults). The birds from both popu-
lations had similar body weight (Bohemian birds—mean 16.5 g ±
0.9 g, N=50; Finnish birds—mean 17.1 g ± 1.0 g, N=50).
The habitats around Konnevesi include mainly sparse mixed
forest with a low undergrowth of moss, grasses and sedges, herba-
ceous plants and shrubs; the forest is interspersed with large clear-
ings including also buildings and human settlements; a brook and
meadows along lake sides are present as well. The Prague locality
consists mainly of large city parks with coniferous and broad-leaved
trees; the parks are surrounded by roads and residential houses with
small patches of ruderal vegetation interspersed. The major park is
an old botanical garden, which represents various Bohemian habi-
tats, and also includes several pools and a small brook. The birds
were trapped in the autumn, when overwintering birds typically
move around (Cepák etal. 2008). Thus, birds in each locality were
likely to be coming from surrounding areas aswell.
Birds were caught using food-baited traps (Central Finland, see
Ham et al. 2006 for details) or mist nets placed near the feeders
(Bohemia) during autumn 2012. They were housed individually in
cages (50 cm × 40 cm × 50 cm in Prague; 65 cm × 50 cm × 80 cm in
Konnevesi) under natural light conditions and were kept on a diet
consisting of mealworms (larvae of Tenebrio molitor L., 1758), pea-
nuts, sunflower seeds and water ad libitum. The birds were allowed
to habituate to the laboratory conditions for 5–7days before the
experiment. Each bird was used only once in each experiment.
After the experiment they were ringed individually and released in
the locality of their capture.
As aposematic prey we used brachypterous adult firebugs [Pyrrhocoris
apterus (L., 1758); Heteroptera], which possess a conspicuous red-
and-black coloration. The species’ defensive secretion from meta-
thoracic glands containing mainly aldehydes (Farine et al. 1992)
makes this insect distasteful for small passerine birds including great
tits (Exnerová et al. 2003). The firebugs live on the ground and
partly also on trees, and feed mainly on seeds of Malvaceae (her-
baceous species and linden tree, Tilia) and locust tree, Robinia pseu-
dacacia (Kristenová etal. 2011; Hotová Svádová etal. 2014). They
are widespread in the Palaearctic but absent in most of Northern
Europe; their range does not exceed the latitude of 60°N (Aukema
and Rieger 2001; Rintala and Rinne 2010).
A nonaposematic variant of the firebugs lacking the red-and-
black color pattern was obtained by painting their upper parts
with dark brown watercolor dye and chalk. We used these color-
manipulated bugs to test the specificity of birds’ reaction toward
the firebugs’ warning coloration, as we needed prey that did not
dier from the aposematic prey in any other trait (size, body shape,
composition of defensive secretion, and so forth). The dye used to
modify the visual part of the firebug warning signal was odorless
and nontoxic, and the chemical defense of these artificially made
nonaposematic firebugs was unchanged (see Exnerová etal. 2003).
The firebugs were collected in Prague (Czech Republic). They were
kept at a temperature of 24 ± 1°C and a light: dark cycle of 16:8 h,
reared on linden seeds (Tilia cordata) and provided with water ad
Mealworms (larvae of Tenebrio molitor) were used as a palatable
control prey to check the foraging motivation of birds before start-
ing a trial with experimental prey. We used nymphs of Jamaican
field crickets [Gryllus assimilis (Fabricius, 1775)] carrying a bright-
blue paper sticker attached to their dorsal side as a novel, edible,
nonaposematic prey to test the level of birds’ food-specific neopho-
bia. The size of crickets oered in experiments matched the aver-
age size of tested firebugs (i.e., 10–12 mm). The sticker covered
most of the cricket’s dorsum, leaving its antennae and legs visible.
In a preliminary experiment (involving 2 other groups of 20 wild-
caught birds, both from Bohemia), great tits hesitated longer before
attacking crickets with a blue sticker (mean 179.2 s ± 28.2, N=20)
than before attacking those without the sticker (mean 40.9 s ± 12.4,
N = 20; Mann–Whitney U-test: Z=−3.92, N= 40, P < 0.001),
which they attacked with similar latencies as familiar mealworms
(mean 24.6 s ± 10.5; Wilcoxon matched pairs test: Z = 1.49,
N =20, P = 0.135). These results indicate that crickets with the
blue sticker represent a stimulus suciently novel to increase attack
Experimental design and equipment
Experiments were designed to compare the exploration behavior,
levels of neophobia, and specific reactions to aposematic and novel
palatable prey between 2 populations of great tits. Each bird was
tested individually in 4 separate tests in the following order, which
was identical for all the birds: 1) exploration test with a novel
object, 2)neophobia test with a novel object placed near the food
bowl, 3)test of reaction toward novel palatable prey, and 4)test of
reaction toward aposematic firebug or its nonaposematic brown-
painted variant. This way the recent aversive experience with fire-
bugs did not aect the reactions of birds toward novel objects and
palatable prey, and the order per se did not influence the compari-
son between populations.
Exploration and neophobiatests
To study exploration behavior and neophobia level we carried out
2 types of novel-object tests: 1)a novel object presented in a neutral
location, and 2)a novel object attached to the food bowl. Anovel
object presented in a neutral location is frequently used to mea-
sure exploration behavior and neophilia, because the bird is not
forced to approach the novel object, and when it does, it indicates
its interest in exploring the object (e.g., Verbeek etal. 1994; Mettke-
Hofmann et al. 2002; Drent et al. 2003). The presentation of a
novel object close to the food bowl is regarded as a measure of neo-
phobia, because it creates a conflict between foraging motivation
and motivation to avoid a novel object; the bird has to overcome
the neophobia to come close to the object and feed (Mettke-
Hofmann et al. 2002; Feenders et al. 2011; Mettke-Hofmann
2012). Although exploration and neophobia may be correlated as
they represent personality traits (van Oers et al. 2004), they are
considered to be 2 distinct responses to novel stimuli (Greenberg
and Mettke-Hofmann 2001).
In the exploration test, we used a bright-blue pen attached
to one of the perches close to the front wall of the home cage.
We measured the latency to peck at the novel object. The test
lasted 10 min (maximum) and was terminated earlier if the bird
pecked at the novel object. Food and water were freely available
at alltimes.
In the neophobia test, we used a pink plastic clothes-peg attached
to the food bowl placed on the home-cage floor. The birds were
deprived of food for 1 h before the test to increase their foraging
motivation. We recorded the latency to feed near the novel object.
The test lasted 10 min and was terminated earlier if the bird started
to feed in presence of the novel object. To control for potential dif-
ferences in foraging motivation, we also carried out a control test
under the same conditions but with the peg absent.
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Behavioral Ecology
Novel and aposematic preytests
Tests with novel palatable prey and firebugs were performed in
experimental cages and followed one after another. Experimental
cages used in Bohemia and in Central Finland were of similar
size (70 cm × 70 cm × 70 cm in Bohemia and 50 cm × 50 cm ×
70 cm in Central Finland); they were made of plywood and a wire
mesh, and equipped with a perch and a water bowl. The front wall
of cages used in Bohemia was made of 1-way glass; the birds in
Central Finland were observed through a small mesh-covered win-
dow in the cage wall. Illumination of the cages simulated the natu-
ral daylight spectrum (including UV wavelengths). The tested prey
was put into the cage in a glass Petri dish placed on a sliding food
tray on the cage floor. Despite of dierence in the cage sizes, the
distance between the food tray and the closest perch was identical
(35 cm). All the prey types appeared conspicuous on the light beige
background of the plywood food tray. Prior to the experiments, the
birds were habituated to the experimental cages, and they were
deprived of food for 2 h to increase their foraging motivation. The
experiments were video-recorded and the birds’ behavior was con-
tinuously registered using Observer XT 8.0 software.
Novel palatable preytest
The novel, palatable, nonaposematic prey was represented by a
Jamaican field cricket with a blue-colored paper sticker attached to
its dorsal side. The experiment consisted of a sequence of 5-min
(maximum duration) trials. At the beginning of the sequence, we
oered the bird a mealworm as a control prey to check its foraging
motivation. When the bird consumed a mealworm, it was oered a
cricket in the subsequent trial. If the bird did not attack the cricket
within the time limit, the sequence continued with another meal-
worm trial followed by another cricket trial up to a maximum of
3 cricket presentations. We measured the latency to attack (touch,
peck, or seize) the cricket and recorded whether the cricket was
killed and eaten.
The birds from both Bohemian and Finnish populations were sub-
divided into 2 experimental groups of 25 birds each, with similar
proportion of yearlings and adults, and males and females. One
group was tested with aposematic red-and-black firebugs, and the
other one with manipulated (brown-painted), nonaposematic (but
still unpalatable) firebugs.
The test consisted of a sequence of alternating trials in which
the birds were presented either with a control prey (mealworms) as
a check of foraging motivation or with a firebug. Each trial lasted
5 min at most, and was terminated earlier if the bird attacked the
prey. The sequence always started with a mealworm trial. When
the bird consumed a mealworm, it was oered a firebug in the
subsequent trial. If the bird did not attack the firebug within the
time limit, the sequence continued up to a maximum of 20 fire-
bug presentations. We measured the latency to approach and attack
(to touch, peck, or seize) the firebug and recorded whether it was
killed, thrown away, or eaten. If the bird attacked one of the fire-
bugs, we kept oering them (alternating with mealworms) until the
bird left untouched 3 firebugs in a row, which was considered an
avoidance-learning criterion.
Data analysis
A Cox hazard regression was used to analyze the dierences
between Bohemian and Finnish great tits in exploration behavior
toward a novel object (the latency to peck at the blue pen) and in
neophobia (the latency to feed in presence of a novel object, the
pink clothes-peg). Locality of bird origin, and bird’s sex and age
were used as explanatory variables. In the analysis of neophobia,
we included the control (peg absent) latencies in the model as a
covariate. The model selection procedure started from the model
including all possible 2-way interactions of locality, age and sex,
and was subsequently simplified. Model selection was conducted
in a hierarchical manner based on the significance of the terms in
A Cox hazard regression was also used to analyze the behavior
of birds to novel palatable prey (cricket with blue sticker), apose-
matic or nonaposematic firebugs, and control familiar prey (meal-
worm oered at the beginning of the experiment). As a response
variable we used latency to attack each prey type (cricket, firebug,
or mealworm). Locality, bird’s sex and age, and in case of firebugs
also their coloration (aposematic, nonaposematic), were used as
explanatory variables. The model selection procedure was similar
to that used for analyzing reaction to a novel object.
We computed Spearman rank correlations between latency to
peck at the novel object in the exploration test, latency to feed in
the presence of novel object in the neophobia test, and latencies to
attack the novel palatable prey and the firebugs. To check whether
the birds considered crickets with blue stickers a novel prey, we
compared attack latencies between crickets and mealworms oered
in the trial preceding the cricket test; the latencies were compared
by Wilcoxon matched pairstest.
We used the number of attacked firebugs before a bird stopped
attacking them as an indicator of learning. A generalized lin-
ear model with Poisson distribution was used to analyze the data.
The model selection was based on significance of the terms in the
model. Bird sex and age, as well as locality of bird origin and fire-
bug coloration, and all possible 2-way interaction terms were used
as explanatory variables. All analyses were conducted using R
2.11.1 and the lme4 package.
Comparison of occurrence of aposematic species
of Heteroptera in Central Europe and Central
Fauna of terrestrial Heteroptera of Central Europe comprises
922 species, 766 (83%) of which are nonaposematic, and 156
(17%) aposematic; in Central Finland 262 (90%) out of 292
species of Heteroptera are nonaposematic, whereas 30 (10%)
are aposematic. Thus, the less speciose fauna of Central
Finland (32% species as compared with Central Europe) has
not only a smaller absolute number of aposematic species (19%
as compared with Central Europe) but also the proportion of
aposematic species in the fauna is 0.59 times smaller than it
should be in accordance with an uniform decrease in species
diversity with increasing latitude (chi square=7.75, df=1, and
Exploration and neophobia
We fitted Cox hazard regression model to explain the variation in
exploration of a novel object (blue pen). However, no significant
dierences between the Bohemian and Finnish birds were detected
(Table1, Figure1). Most birds approached the object and pecked at
it within the time limit. The average pecking latency was 325 ± 21.5
s (N=100).
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Exneroetal. • Geographic dierences in behavior toward aposematicprey
Our final Cox hazard regression model explaining the birds’
latency to feed in proximity of a novel object (pink peg) included
locality, bird age, and the interaction of both (Figure1, Table2). In
general, Finnish birds hesitated longer compared with those from
Bohemia. Among all the birds, Bohemian adults were the least neo-
phobic, which caused the eect of the interaction between locality
and age of birds (Figure1, Table2).
Latencies measured in exploration and neophobia tests were
significantly correlated in birds from both populations (Finnish
birds: r
=0.60, t=5.15, df=48, and P<0.05; Bohemian birds:
=0.29, t=2.10, df=48, and P<0.05).
Reaction to novel palatableprey
Most birds attacked the novel palatable prey (blue cricket) in the
first or second trial (mean 357 ± 37.2 s, N=100). The birds from
both localities hesitated longer before attacking the blue crick-
ets than before attacking familiar mealworms (Wilcoxon matched
pairs test: Finnish birds, Z=5.56, N=50, and P<0.01; Bohemian
birds, Z=5.23, N=50, and P <0.01).
No significant eect of locality of bird origin was found explain-
ing the variation in attack latencies (Figure2, Table3). However,
nonsignificant trend for adult birds to be less hesitant than yearlings
was detected (Table3). We did not find a significant eect explain-
ing the variation in latency to attack the mealworm oered just
before the novel-prey test either (all P values of main eects (local-
ity, age, sex) and their interactions were > 0.230); this indicates that
all the birds entered the test with similar foraging motivation.
Attack latencies did not correlate with the latencies measured
in exploration (Finnish birds: r
= 0.04, t = 0.27, df = 48, NS;
Bohemian birds: r
=0.02, t=0.12, df=48, NS) and neophobia
(Finnish birds: r
= 0.06, t=0.40, df= 48, NS; Bohemian birds:
=0.16, t=1.10, df=48, NS) tests.
Reaction to aposematic and nonaposematic
A similar proportion of Finnish and Bohemian birds attacked
nonaposematic firebugs (chi square=1.75, df=1, and P=0.185).
Aposematic firebugs were mostly attacked by Finnish birds, and
mostly avoided by Bohemian birds (chi square=8.33, df=1, and
Fitting Cox hazard regression describing exploration of a novel
object (latency to peck at a blue pen) in Bohemian and Central
Finnish great tits
Model Term removed df P
Sex*age + age*locality +
Sex*age 1 0.9036
Age*locality + sex*locality Locality*age 1 0.5712
Age + locality + sex + sex*locality Sex*locality 1 0.4664
Age + locality + sex Age 1 0.5506
Locality + sex Sex 1 0.6572
Locality 1 0.0897
When an interaction is indicated (*), the main eect of the term is also
included in the model. Degrees of freedom and significances are given for the
excluded term in the model.
Central Finland Bohemia
Exploration test
Neophobia test
Latency (s) (Mean +/- SE)
Latency of Bohemian and Central Finnish great tits to peck at a novel object
(blue pen; exploration test; open bars) and their latency to start feeding after
a novel object was attached to the food bowl (pink peg; neophobia test; gray
Cox regression model explaining latency of Bohemian and
Central Finnish great tits to start feeding after a novel object
was attached to the food bowl (pink peg; neophobia test)
Source Coef. SE z P
Locality (Bohemia) 1.336 0.293 4.565 <0.001
Age (juv.) −0.039 0.377 −0.103 0.918
Sex (males) −0.002 0.998 −0.010 0.992
Locality (Bohemia): age (juv.) −0.950 0.519 −1.827 0.068
Interaction terms of the sex and age, and the locality and sex were removed
from the model because they were not significant (z < ±1, P > 0.36).
Blue cricket
Nonaposematic firebug
Aposematic firebug
Latency to attack (s) (Mean +/- SE)
Central Finland Bohemia
Latency of Bohemian and Central Finnish great tits to attack a novel prey
(cricket with a blue sticker; open bars), nonaposematic firebug (brown-
painted; light gray bars), and aposematic red-and-black firebug (wild-type;
dark gray bars).
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Behavioral Ecology
Cox hazard regression model explaining the variation in latencies
to attack the firebugs revealed a significant interaction between firebug
coloration and the locality of bird origin (chi square= 3.95, df= 1,
and P=0.047). Other terms included in the model were: locality, age
and sex of the bird, and firebug coloration. Bohemian birds were more
hesitant to attack aposematic firebugs than Finnish birds, but there was
no dierence in latencies to attack nonaposematic firebugs (Figure2).
In Finnish birds, the latencies to attack both aposematic and
nonaposematic firebugs correlated with the latencies to attack
novel palatable prey (aposematic bugs: r
=0.46, t=2.46, df=23,
and P < 0.05; nonaposematic bugs: r
=0.61, t=3.65, df=23, and
P<0.05); for Bohemian birds no such correlation was found (apo-
sematic bugs: r
=0.10, t=0.49, df=23, NS; nonaposematic bugs:
=0.26, t=1.27, df=23,NS).
General linear model explaining the number of attacked firebugs
comprised locality of bird origin, bird sex, and firebug coloration
and the interactions between locality and firebug coloration, and
bird sex and firebug coloration (Table4, Figure3). The significant
interaction between firebug coloration and locality arose from the
fact that Bohemian birds attacked more nonaposematic firebugs
than aposematic ones, whereas Finnish birds attacked similar num-
bers of both color forms (Table5, Figure3). Interestingly, in both
localities, males tended to attack more aposematic firebugs than
females. Individual females usually did not attack more than a sin-
gle firebug (mean 1.2 ± 0.6, N=41), whereas the males frequently
attacked 2 and more (up to 4)individuals (mean 1.6 ± 0.7, N=59).
Environmental factors, particularly food availability and predators,
are suggested to be the main drivers selecting for dierences in forag-
ing behavior among local bird populations (e.g., Shochat etal. 2004).
However, we still have very limited understanding of how such dier-
ences arise, and whether certain behavioral traits are selected together
or independently. We compared several foraging-related traits in 2 geo-
graphically distant populations of great tits. Those populations have
presumably experienced dierent selective environments in terms of
habitats, diversity and abundance of noxious prey. Although our exper-
iments are not able to discern whether the observed dierences already
reflect local adaptations or whether they reflect dierences in experi-
ence, our results raise some interesting points regarding the nature of
dierences in the reaction of wild-caught birds to aposematic prey and
how they are correlated with exploration behavior and neophobia.
Exploration and neophobia—comparison of
Finnish and Bohemianbirds
Finnish and Bohemian great tits did not dier in their tendency to
explore a novel object placed in a neutral location in their home
Model fitting of Poisson GLM explaining the number of firebugs
(either aposematic or nonaposematic) attacked by Bohemian
and Central Finnish great tits
Model Term removed df P
Locality * sex + locality * age + locality *
color + age * color + sex * color
Age * color 1 0.9811
Locality * sex + locality * age + age * color
+ sex * color
Locality * age 1 0.8621
Locality * sex + age * color + sex * color Locality * sex 1 0.8452
Age + locality + sex + color + locality *
color + sex * color
Age 1 0.5427
Locality + sex + color + locality *
color + sex * color
If interaction is indicated (*), the main eect of the term is also included in the
model. Degrees of freedom and significances are given for the excluded term
in the model. Our final model (see details in Table5) is highlighted in bold.
Central Finland Bohemia
Number of firebugs attacked (Mean + SE)
Dierence between Bohemian and Central Finnish great tits in the number
of nonaposematic and aposematic firebugs attacked.
Poisson GLM explaining number of firebugs attacked by
Bohemian and Central Finnish great tits
Source Estimate SE z P
Intercept 0.3400 0.2228 1.526 0.1270
Locality −0.1476 0.2635 −0.560 0.5753
Sex −0.2353 0.2630 −0.895 0.3710
Color −0.9606 0.4733 −2.029 0.0424
Locality * color −1.2795 0.5254 −2.435 0.0149
Sex * color 1.0870 0.5252 2.070 0.0385
Eects of factor levels locality (Central Finland), sex (female), and firebug
color (nonaposematic) are included in the intercept.
Fitting Cox hazard regression describing latency of Bohemian
and Central Finnish great tits to attack a novel palatable prey
(blue cricket)
Model Term removed df P
Sex * age + age * locality +
sex * locality
Age * locality 1 0.9049
Sex * age + sex * locality Sex * locality 1 0.3953
Age + sex + locality + sex * age Locality 1 0.9588
Age + sex + sex * age Sex * age 1 0.2273
Age + sex Sex 1 0.3675
Age 1 0.1283
When an interaction is indicated (*), the main eect of the term is also
included in the model. Degrees of freedom and significances are given for
the excluded term in the model.
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Exneroetal. • Geographic dierences in behavior toward aposematicprey
cage. However, Finnish birds appeared more neophobic, and hesi-
tated longer than Bohemian birds before starting to feed next to a
novel object attached to their food bowl. Our results suggest that
environmental conditions both in Bohemia and Central Finland
may, in spite of their dierences, favor similar exploration tenden-
cies in great tit populations. Similarly, Miranda etal. (2013) did not
find any dierences in novel object exploration between 2 popu-
lations of European blackbirds (Turdus merula) living in dierent
The extent of object neophobia has been frequently found to
dier between conspecific populations (e.g., Martin and Fitzgerald
2005; Mettke-Hofmann et al. 2013; Miranda etal. 2013, but see
Echeverría and Vassallo 2008; Bókony et al. 2012). Several fac-
tors may explain the greater object neophobia of Finnish great
tits in our experiment. First, Finnish birds may be more cautious
to approach novel objects near their feeding place due to greater
vigilance caused by higher frequency of potential predators as can
be expected in a less populated and more natural landscape. In
sticklebacks (Gasterosteus aculeatus), individuals living in areas with
greater predation pressure are less bold and more neophobic than
those inhabiting areas with less predators (Bell 2005; Dingemanse
etal. 2007; Brydges etal. 2008). Second, Finnish birds may exhibit
greater object neophobia because of a larger proportion of migrat-
ing individuals (Cepák etal. 2008). Although the great tit is mostly
a resident species, some individuals (mostly yearlings) undergo
short-distance autumnal migration (Cramp and Perrins 1993).
Greater neophobia of birds from migratory populations than from
the resident ones has been found in 2 New World blackbird spe-
cies (red-winged blackbird Agelaius phoeniceus and Brewer’s blackbird
Euphagus cyanocephalus); the dierence may have been caused by
residents having higher costs of missing new opportunities in the
seasonally changing environment (Mettke-Hofmann et al. 2013).
Lesser neophobia of Bohemian birds may be also partly explained
by their more urbanized locality. Birds from urban populations may
be bolder and less neophobic than their rural conspecifics, as is the
case in European blackbirds (Turdus merula; Miranda et al. 2013),
and song sparrows (Melospiza melodia; Evans etal. 2010).
Behavior of Finnish and Bohemian birds toward
novel palatableprey
Finnish and Bohemian great tits did not dier in their behav-
ior toward a novel palatable prey, the cricket with a blue sticker
attached. They attacked the crickets with similar latencies, and
mostly killed and consumed them. This suggests that the hesita-
tion behavior toward novel prey does not reflect any general dif-
ference in local prey communities and frequency of potentially
Surprisingly, we did not find any correlation between the behav-
ior of birds toward novel prey and their reaction to novel objects
(exploration and neophobia) in the 2 populations studied. In juve-
nile Dutch great tits coming from lines selected for opposed person-
ality traits (Drent etal. 2003), the generally more neophobic “slow
explorers” hesitated longer before attacking novel prey (red-and-
black firebugs) than the less neophobic “fast explorers” (Exnerová
et al. 2010). There are several mutually nonexclusive factors pos-
sibly responsible for the dierence between the results of our pres-
ent and previous studies (Exnerová et al. 2010): 1) The inherited
correlation between food neophobia and object neophobia may be
prominent in naive juvenile birds. In contrast, adult wild-caught
individuals may not show such a correlation due to their experi-
ence with various types of both palatable and unpalatable prey, as
well as experience with food shortage periods. In wild-caught tits
living outside the breeding season in small flocks, the food neo-
phobia may also be influenced by the position of an individual in
the flock hierarchy (Farine etal. 2015). In black-capped chickadees
(Poecile atricapillus), for instance, subordinate individuals are less neo-
phobic than dominant ones (An et al. 2011). 2) The correlation
may be more apparent in birds coming from the lines selected for
the opposed personalities (Drent et al. 2003), than in birds from
natural populations with possibly less extreme values of personality
traits. 3)Food neophobia may be correlated with other personality
traits in some populations (Dutch; Exnerová etal. 2010), but not
in others (Finnish and Bohemian, this study). Bókony etal. (2012)
found that food neophobia in house sparrows (Passer domesticus) cor-
related with activity, risk-taking, and object neophobia only in 1 of
4 Hungarian populations studied. In Kenya none of the 8 popu-
lations of house sparrows tested showed any relationship between
exploration of a novel object and consumption of novel food (Liebl
and Martin 2014).
Reactions of Finnish and Bohemian birds toward
The behavior of birds toward firebugs was aected by the firebug
coloration. In contrast to behavior toward novel palatable prey, the
Finnish birds partly diered from the Bohemian birds in their reac-
tions. Nonaposematic firebugs were attacked in similar proportions
by Finnish and Bohemian birds. The birds from both populations
also hesitated about the same time before attacking nonaposematic
firebugs, and learned to avoid them at a similar rate. In Finnish
birds, the attack latencies for nonaposematic firebugs correlated
with those for novel palatable prey, whereas in Bohemian birds the
latencies were not correlated. These results indicate that nonapo-
sematic, brown-painted firebugs were novel for Finnish birds, and
that the reaction to them followed the general behavior of birds
toward a novel prey. Noncorrelated latencies of Bohemian birds
suggest that these birds may be experienced with some similar,
nonaposematic but unpalatable true bugs from the wild (e.g., some
species of Rhyparochromidae), and that they partly generalized
their experience. On the other hand, the Bohemian birds attacked
nonaposematic firebugs more frequently than the aposematic ones,
which confirms the results of previous studies (Exnerová et al.
2003, 2006) suggesting that the characteristic red-and-black color
pattern of firebugs facilitates their recognition by avian predators.
The Finnish and Bohemian great tits significantly diered in
their behavior toward aposematic firebugs. Most Bohemian birds
avoided them on sight, whereas most Finnish birds attacked at least
1 individual. Finnish birds generally behaved toward aposematic
firebugs in a similar way as to the nonaposematic ones, and their
initial reactions (before the first contact with firebug defense chemi-
cals) were correlated with their reactions to palatable prey of novel
appearance (blue crickets). The dierences in behavior toward the
aposematic firebugs did not follow the dierences between the 2
populations in exploration and neophobia. Birds from both popula-
tions behaved similarly in response to a novel object and to a novel
palatable prey, and the only dierence—hesitation to feed in pres-
ence of a novel object—does not correspond with behavior toward
the aposematic prey, because the Finnish birds were more neopho-
bic. Therefore, the dierence in avoidance between the wild-caught
Finnish and Bohemian great tits is likely to be the result of indi-
vidual learning and their dierent experiences in thewild.
Although the Finnish birds attacked aposematic firebugs more
frequently than the Bohemian birds, it is interesting that the
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Behavioral Ecology
Finnish birds stopped attacking them on average after only 1 trial.
This means that the Finnish wild-caught birds learned to avoid the
novel aposematic firebugs considerably faster than the conspecific
naive hand-reared birds from Bohemia, which attacked on aver-
age 5 firebugs (Svádová etal. 2009) before learning to avoid them.
This dierence suggests that the Finnish wild-caught birds may
have generalized their previous experience with some unpalatable
defended prey, even of a dierent appearance than firebugs, and
this may have increased their avoidance learningrate.
Alternatively, the dierence may suggest an innate bias against
conspicuous aposematic prey (Lindström etal. 1999a), which can
speed up avoidance learning. Avoidance learning against an apo-
sematic prey that is evolutionarily novel needs typically several
unpleasant experiences before the novel prey is learned to be
avoided (e.g., Mappes and Alatalo 1997; Lindström et al. 1999b).
In previous studies, naive juvenile great tits did not hesitate longer
before attacking aposematic than nonaposematic prey (Svádová
et al. 2009), but they showed an innate bias against aposematic
prey, when the nonaposematic (Lindström etal. 1999a) or less con-
spicuous (Fabricant etal. 2014) alternative prey was present. These
2 alternatives are not mutually exclusive, and the reactions observed
in wild-caught birds are likely the result of an interaction between
an innate bias and individual experience. Assessing the eect of
both processes would, however, require further experiments with
naive predators and the use of the prey novel for both populations.
For the nonaposematic firebugs, the learning rates were similar in
Bohemian and Finnish birds, indicating that the populations do not
dier in their ability to learn avoiding unpalatable prey. The Finnish
birds, for which both firebug color forms were novel, learned to
avoid red-and-black and brown-painted firebugs at a similar rate.
This agrees with previous studies with great tits and defended con-
spicuous prey where learning rate between “typical” warning colors
versus gray or brown did not dier (Ham etal. 2006; Svádová etal.
2009). Because our experiment was designed mainly to test the
attack willingness toward the aposematic prey, rather than learn-
ing abilities, we are unable to make any strong conclusions about
the general dierences in learning abilities between populations.
Furthermore, we compared an experienced population to a naive
one. In the future, it would be interesting to compare learning abili-
ties between populations by using a completely novel aposematic
prey and/or naivebirds.
Our results indicate a stronger avoidance of aposematic bugs
by female great tits than by males. Similar results were obtained
in a study where female bobwhites (Colinus virginianus) showed more
aversion than males toward red- and orange-dyed food (Mastrota
and Mench 1994). Adierent study with the same species however,
found no dierences between the sexes in color aversion, presum-
ably because the individuals used in both experiments diered in
age (Mastrota and Mench 1995). Color aversion in females, but not
in males, seems to increase with age (Mastrota and Mench 1994).
Apossible explanation is that females consume more insects than
males, and they teach chicks to avoid toxic prey. Whether this is the
case for great tits is a matter of future research.
Aposematic Heteroptera and other insects of
Central Finland as potentialmodels
Wild-caught great tits are potentially experienced with an unknown
number of both palatable and unpalatable species of insects,
both in Central Finland (around the 62°N latitude) and Bohemia.
Unfortunately, there are no data available to compare the abun-
dance and diversity of potential insect prey between the 2 areas.
However, because the reactions of the birds toward the firebug
were specific, we consider the evaluation of heteropteran faunas
informative, as it compares the numbers of potential models the
birds may be experienced with from thewild.
We have documented that the fauna of aposematic terrestrial
Heteroptera of Central Finland is much less diverse than that
of Central Europe both in absolute and relative number of spe-
cies (30 vs. 156 species, 10% vs. 17% of total faunas, respectively).
The Bohemian great tits are certainly experienced with Pyrrhocoris
apterus due to the frequent occurrence of the bug, its aggregations
and its ubiquitous host plants (Exnerová et al. 2006); these birds
can be potentially experienced with other chemically protected red-
and-black true bug species as well (Hotová Svádová et al. 2010).
Although P. apterus does not occur in Central Finland (Rintala and
Rinne 2010), we cannot exclude a priori the local occurrence of
insect species that the birds would generalize with. However, the
other Finnish similarly colored aposematic insects are either too
rare (Corizus hyoscyami, Rhopalidae), or look too dierent (plant bugs,
Miridae; burnet moths, Zygaenidae; ladybird beetles, Coccinellidae)
to function as models for generalization with red-and-black fire-
bugs. Moreover, recent analysis of Finnish Lepidoptera showed
that only less than 5% of caterpillars are aposematic (Mappes etal.
2014). It is still possible that the negative experience with some of
the above taxa may have played a role in the generalization of the
firebug color patterns as great tits have been shown to generalize
their learned avoidance among colors (red, yellow, and orange;
Ham etal. 2006), among aposematic species (Hotová Svádová etal.
2013) and between bi-chromatic symbols (Ihalainen etal. 2008).
Even though a broader generalization of our results is limited
by the study of only 2 populations, we have shown that conspe-
cific birds from 2 geographically distant populations may express
similar reactions to a prey which is novel for both of them. In
our case, food neophobia was low in both populations, whereas
the avoidance of aposematic prey was dierent between the
populations, and could be explained by dierences in experience.
Bohemian birds have plenty of opportunities to meet firebugs in
their natural environment and learn about their unpalatability;
Finnish birds do not have such opportunity. Our results emphasize
that naive birds’ tendency to attack novel aposematic prey may
have important implications for range extensions of prey species.
We can not tell whether the dierence in avoidance was a result
of Finnish birds’ lower experience with any aposematic prey, or
whether the avoidance learning is prey specific. Our results indi-
cate, however, that studies on aposematism and mimicry based on
geographically distant conspecific populations can be compared
and generalized.
This work was supported by the Czech Science Foundation
(P505/11/1459 to A.E., D.J., P.Š., and L.D.) and the Finnish
Centre of Excellence in Biological Interactions (252411 to J.M.).
We are deeply grateful to H.Nisu for her help with the birds at Konnevesi
Research Station, and to J.Valkonen and A.Lopez-Sepulcre for invaluable
help with statistical analyses. We thank editors and 3 anonymous referees
for helpful comments and suggestions on the manuscript.
Handling editor: Alison Bell
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... Most frequently tested passerine species include great tits (Parus major; Ihalainen et al., 2012;Lindström et al., 1997), blue tits (Cyanistes caeruleus; Aronsson & Gamberale-Stille, 2013) and starlings (Sturnus vulgaris; Skelhorn & Rowe, 2009). Moreover, the experiments involve both wild-caught adults (Exnerová et al., 2015) and hand-reared juveniles (Exnerová et al., 2010;Lindström et al., 1999) as model avian predators. ...
... We found differences between males and females in their performance in the colour discrimination task, with females performing better than males in the memory test. Stronger avoidance of aposematic prey in females than in males was found also in another study testing great tits (Exnerová et al., 2015). Likewise, female bobwhites Colinus virginianus showed stronger avoidance of red and orange food than did the males (Mastrota & Mench, 1994). ...
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When learning to discriminate between palatable and unpalatable prey, predators may encounter the prey either simultaneously or in a sequence. The two types of discrimination tasks, which are frequently used in experiments focused on aposematism and mimicry, may considerably differ in difficulty, as they differ in the information available to predators during individual encounters with prey. Surprisingly, there are very few studies directly comparing the performance of predators between sequential and simultaneous discrimination tasks using otherwise identical experimental design, the same predators and prey. We tested the effect of the type of discrimination task on the effectiveness of discrimination learning in adult and juvenile great tits ( Parus major ). Birds were trained to discriminate between palatable and unpalatable artificial prey items baited with mealworms soaked either in water or quinine. Prey shape, colours and patterns were derived from real shield bug species. We compared the performance of birds tested with two discriminative cues, colour and pattern, using three discrimination tasks: (1) sequential—alternating presentation of one palatable and one unpalatable prey item, (2) two‐choice—simultaneous presentation of one palatable and one unpalatable prey item and (3) multiple‐choice—simultaneous presentation of multiple palatable and unpalatable prey items. Colour was a more effective discriminative cue than pattern for both adult and juvenile birds. Adults performed better than juveniles regardless of task. The birds performed equally well in the sequential and two‐choice tasks, but their performance in the multiple‐choice task was worse than in the other two tasks. However, these differences were only present when the birds used the pattern as a discriminative cue. The birds tested with colour, a more salient cue, performed equally well in all three tasks. Type of discrimination task may therefore affect the learning performance of predators, but the effect also depends on the saliency of a particular discriminative cue.
... If the chick attacked the mealworm upon the frog model, the sequence continued up to a maximum of ten presentations of the frog model. When the chick refused to attack the mealworm upon the frog model for three consecutive presentations, the chick was considered to ESI = ∑ (prey score)(weight by attack order) total number of attacks made by the chick in the learning session have learned to avoid the prey through the association between the warning coloration and the unpleasant taste of the mealworm (Exnerová et al 2015;Lawrence et al 2019). ...
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Aposematism is an anti-predator strategy where predators learn to associate the warning signal on prey with an unpleasant experience, and consequently, avoid attacking similar prey in the future. Conspicuous coloration in poison frogs (Dendrobatidae) is considered a warning signal. During parental care, parents transport their tadpoles on the dorsum, which could alter the detectability and recognition of such warning coloration by visually oriented predators. We tested this hypothesis using domestic chicks trained to avoid and discriminate between printed frog models with and without conspicuous-warning coloration. We tested whether the chicks recognized the warning coloration on printed frog models that varied in the quantity of tadpoles on the dorsum. Chicks first attacked frog models without warning coloration, whether they had tadpoles on the dorsum or not. In contrast, frog models with warning coloration were attacked last by chicks. Moreover, the frog models with warning coloration and without tadpoles experienced a lower risk of attack by chicks than similar frog models with tadpoles. However, aposematic frog models maintained the warning function of conspicuous coloration if it was located on parts of the parent's body that are not covered by the tadpoles when transported. Our results suggest that tadpoles on the dorsum of parents might compromise the effectiveness of the warning signal display in poison frogs increasing the risk of attack by visually oriented predators.
... Variation in coloration is likely to be maintained through the joint effect of several mechanisms, making it hard to detect their individual effects. There are reports describing the effects of heterozygote advantage, variation in predators at different levels, socially transmitted avoidance, signaling trade-offs, among others as mechanisms facilitating variation in coloration and/or color polymorphism (Exnerová et al. 2010(Exnerová et al. , 2015Nokelainen et al. 2014;Willmott et al. 2017;Thorogood et al. 2018). There is no reason to believe mechanisms that influence success of visual cues act in isolation from each other. ...
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A big question in behavioral ecology is what drives diversity of color signals. One possible explanation is that environmental conditions, such as light environment, may alter visual signaling of prey, which could affect predator decision-making. Here, we tested the context-dependent predator selection on prey coloration. In the first experiment, we tested detectability of artificial visual stimuli to blue tits (Cyanistes caeruleus) by manipulating stimulus luminance and chromatic context of the background. We expected the presence of the chromatic context to facilitate faster target detection. As expected, blue tits found targets on chromatic yellow background faster than on achromatic grey background whereas in the latter, targets were found with smaller contrast differences to the background. In the second experiment, we tested the effect of two light environments on the survival of aposematic, color polymorphic wood tiger moth (Arctia plantaginis). As luminance contrast should be more detectable than chromatic contrast in low light intensities, we expected birds, if they find the moths aversive, to avoid the white morph which is more conspicuous than the yellow morph in low light (and vice versa in bright light). Alternatively, birds may attack first moths that are more detectable. We found birds to attack yellow moths first in low light conditions, whereas white moths were attacked first more frequently in bright light conditions. Our results show that light environments affect predator foraging decisions, which may facilitate context-dependent selection on visual signals and diversity of prey phenotypes in the wild.
... These are common spiders at our localities, and we may expect tested great tits to be familiar with them as a common and palatable prey 27,28 . A baseline prey was represented by juveniles of the Mediterranean cricket, which are commonly accepted as artificial insect prey by great tits 35 . ...
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Myrmecomorphy is a strategy utilized by a variety of species, among which spiders are the most common. It is supposed that myrmecomorphy tends to be selected by predator avoidance of preying on ants rather than by blind ant workers. To date, this hypothesis has been tested mainly on invertebrate predators (mantises and spiders). We are the first to test whether an imperfect myrmecomorph spider (Phrurolithus festivus) gains protection against avian predators (wild adult great tits—Parus major) through its appearance. In a set of preferential trials, we showed that the ant model and the myrmecomorph spider are equally well protected against attack, though the attacked myrmecomorphs are usually eaten. This suggests that the mimicry of the myrmecomorph spiders is effective against avian predators and works in a Batesian manner. In this study, we have provided evidence toward the evolution of myrmecomorphy in response to selective pressure elicited by visually-oriented predators like birds.
... However, separating cause and effect can be difficult, is the white morph more prevalent in central Finland because it has an advantage against the local predators, or has the previous experience of the predators with the white-biased population pre-conditioned them to show greater avoidance of the white morph when common? Evidence has been found for population level differences in great tit behavior towards aposematic prey (Exnerová et al., 2015), suggesting that even within a single predator species, predator variation may affect the outcome of studies such as ours. One way to examine this would be to repeat this experiment at other locations known to vary in morph frequencies. ...
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Polymorphic warning signals in aposematic systems are enigmatic because predator learning should favor the most common form, creating positive frequency-dependent survival. However, many populations exhibit variation in warning signals. There are various selective mechanisms that can counter positive frequency-dependent selection and lead to temporal or spatial warning signal diversification. Examining these mechanisms and their effects requires first confirming whether the most common morphs are favored at both local and regional scales. Empirical examples of this are uncommon and often include potentially confounding factors, such as a lack of knowledge of predator identity and behavior. We tested how bird behavior influences the survival of three coexisting morphs of the aposematic wood tiger moth Arctia plantaginis offered to a sympatric predator (great tit Parus major) at different frequencies. We found that although positive frequency-dependent selection is present, its strength is affected by predator characteristics and varying prey profitability. These results highlight the need to understand predator foraging in natural communities with variable prey defenses in order to better examine how behavioral interactions shape evolutionary outcomes.
... Although predators of aquatic nymphs could not be considered candidate agents of selection for aposematic colouration in the terrestrial adult stage, it is common for experimental predators to be used for testing recognition and avoidance of unpalatable prey (e.g. Darst & Cummings 2006;Prudic et al. 2007;Exnerová et al. 2015). We therefore consider that predator aversiveness towards the nymph stage of an austroperlid species would be satisfactory evidence for unpalatability, such that conspicuous colouration exhibited in the adult stage of that same species could be considered to serve an aposematic function. ...
Aposematism is a phenomenon in which defended prey advertise their unprofitability to predators through conspicuous signals. Aposematic (warning) colouration is widespread across numerous insect orders but rarely occurs in insects that inhabit aquatic environments where conditions can impose constraints on visual signal transmission. In the semi-aquatic insect order Plecoptera (stoneflies), only the terrestrial adult stage of Austroperla cyrene (Austroperlidae) from New Zealand has been suggested to possess aposematic colouration, associated with the presence of hydrogen cyanide and documented unpalatability to predators. Here, we review evidence for the occurrence of aposematic colouration in Australian and South American Austroperlidae based on a synthesis of taxonomic literature and studies examining feeding preferences of predators in aquatic environments. Contrasting black, white and yellow colouration occurs commonly in adult Austroperlidae, and nymphs of several surveyed species were found to be aversive to predators, together suggesting that aposematism may be widespread in this family. The wider prevalence of aposematism in Austroperlidae should be examined further by directly testing the palatability of various species to predators and by analysing the chemical compositions of their defensive secretions. Austroperlid stoneflies offer new potential for understanding the evolution of aposematism in ecological and phylogenetic contexts that have not yet been explored.
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Insect herbivores and their parasitoids play a crucial role in terrestrial trophic interactions in tropical forests. These interactions occur across the entire vertical gradient of the forest. This study compares how caterpillar communities, and their parasitism rates, vary across vertical strata and between caterpillar defensive strategies in a semi deciduous tropical forest in Nditam, Cameroon. Within a 0.1 ha plot, all trees with a diameter at breast height (DBH) ≥ 5 cm were felled and systematically searched for caterpillars. We divided the entire vertical gradient of the forest into eight, five-meter strata. All caterpillars were assigned to a stratum based on their collection height, reared, identified, and classified into one of three defensive traits: aposematic, cryptic and shelter-building. Caterpillar species richness and diversity showed a midstory peak, whereas density followed the opposite pattern, decreasing in the midstory and then increasing towards the highest strata. This trend was driven by some highly dense shelter-building caterpillars in the upper-canopy. Specialisation indices indicated decreasing levels of caterpillar generality with increasing height, a midstory peak in vulnerability, and increasing connectance towards the upper-canopy, although the latter was likely driven by decreasing network size. Both aposematic and shelter-building caterpillars had significantly higher parasitism rates than cryptic caterpillars. Our results highlight nuanced changes in caterpillar communities across forest strata and provide evidence that defences strategies are important indicators of parasitism rates in caterpillars and that both aposematic and shelter-building caterpillars could be considered a “ safe haven” for parasitoids.
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The study of consistent individual differences has become an important focus in research on animal behaviour. These behavioural differences are typically measured through standardized testing procedures. One frequently used paradigm is the novel object test, in which animals are exposed to unfamiliar objects and their reaction is quantified. We used meta-analysis to evaluate how reliably novel object trials quantify individual differences. Overall, we found repeatability of responses to novel objects was strong and significant and was larger in short-term than in long-term studies. Average sample size and long-term estimates have both increased over the past three decades. Most short-term studies used different novel objects in repeated presentations, while long-term studies used either the same or different novel objects almost equally often. Novelty, the time interval between trials and their interaction together explained little of the total heterogeneity, while between-study heterogeneity remained large. Overall, novel object trials reliably estimate individual differences in behaviour, but results were very heterogeneous even within the same study species, suggesting susceptibility to unknown details in test conditions. Most studies that use novel object trials in a foraging context label the trait as neophobia, while novel object trials in a neutral context are labelled variously as shyness–boldness, exploration–avoidance or neophilia. To avoid ambiguity, we argue for the use of object–neophobia for trials near resources and object–neophilia for trials in a neutral context as the most specific labels for novel object responses.
Pyrrhocoroidea represents an important group of true bugs (Insecta: Hemiptera: Heteroptera) which includes fire bugs, cotton stainers and other taxa widely used in experimental studies or known as pests. However, the morphology and phylogeny of Pyrrhocoroidea have been only poorly studied so far. Here, structures of the external scent efferent system of the metathoracic scent glands are examined in 64 out of 71 currently valid genera of Pyrrhocoroidea and scanning electron micrographs are provided for most taxa. Several characters are revealed which define each of the three higher taxa within Pyrrhocoroidea: Larginae (small auriculate peritreme lacking manubrium and median furrow; metathoracic spiracle never surrounded by evaporatorium), Physopeltinae (large, widely open ostiole; large peritremal disc with manubrium [new term], lacking median furrow; mace-like mycoid filter processes of equal shape and size on both anterior and posterior margins of metathoracic spiracle), and Pyrrhocoridae (elongate auriculate peritreme with deep median furrow). Within Pyrrhocoridae, three main types (A, B and C) of the external scent efferent system are distinguished, differring in the amount of reductions. The findings are interpreted in the context of phylogenetic hypotheses available for Pyrrhocoroidea and their close relatives, Coreoidea and Lygaeoidea. An updated identification key to the families and subfamilies of Pyrrhocoroidea applicable for both sexes is provided.
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Batesian mimicry involves both spatial and temporal interactions between model, mimic and predator. Fundamental predictions in Batesian mimicry involve space, time and abundance; specifically, that the model and mimic are found in sympatry and that protection for the mimic is increased when predators interact with the model first and more frequently. Research has generally confirmed these predictions for Batesian mimicry at large spatial scales, with recent work on two nymphalid butterflies in western North America, the mimic Limenitis lorquini (Boisduval, 1852) and its model Adelpha californica (Butler, 1865) in western North America indicating that the mimic generally has lower abundance and emerges later in the season among widely separated populations in the California Coast Ranges and Sierra Nevada. However, no studies have investigated model–mimic dynamics at small scales in the temperate zone to test whether temporal habitat use and movements conform to predictions. If mimicry is as important a part of the biology of these temperate species as it is for their tropical counterparts, then in addition to emerging later and being less abundant overall, the mimic should be less widespread, should be less abundant in each habitat and should move less among available habitats. Our results using mark–release–recapture methods confirm these predictions and indicate that the mimic, L. lorquini, is enjoying an umbrella of protection against habitat specialist and generalist predators alike.
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Supplement to the Catalogue of the Heteroptera of the Palaearctic Region volume 1-5. Data available at
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The populations of the firebug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) in Europe exhibit three kinds of host plant associations: feeding on seeds of (1) Tilia spp. (Tiliaceae), (2) Malvaceae (s. str.), and (3) Robinia pseudacacia (Fabaceae). The three host plant taxa often grow in different habitats and localities. We have tested the hypothesis that P. apterus forms on different host plants specialised "trophic populations" which also influence its food preference. We have collected P. apterus from localities with Tilia platyphyllos, Malva neglecta or Robinia pseudacacia as host plants and tested their preferences in a multiple choice test involving seeds of Tilia cordata, T. platyphyllos, Althaea officinalis, Alcea rosea and Robinia pseudacacia. The original host plant of P. apterus population had no influence on food preferences. However, the preferences differed between adults and the third instar larvae. The adults preferred seeds of Robinia pseudacacia followed by Althaea officinalis, while the preferences of larvae were less pronounced and ranked in order Althaea officinalis, Robinia pseudacacia, and Tilia platyphyllos. Existence of trophic populations of P. apterus was not confirmed by our experiment. Durations of feeding were longer on preferred species of seeds in both adults and larvae.
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Understanding the functional links between social structure and population processes is a central aim of evolutionary ecology. Multiple types of interactions can be represented by networks drawn for the same population, such as kinship, dominance or affiliative networks, but the relative importance of alternative networks in modulating population processes may not be clear. We illustrate this problem, and a solution, by developing a framework for testing the importance of different types of association in facilitating the transmission of information. We apply this framework to experimental data from wild songbirds that form mixed-species flocks, recording the arrival (patch discovery) of individuals to novel foraging sites. We tested whether intraspecific and interspecific social networks predicted the spread of information about novel food sites, and found that both contributed to transmission. The likelihood of acquiring information per unit of connection to knowledgeable individuals increased 22-fold for conspecifics, and 12-fold for heterospecifics. We also found that species varied in how much information they produced, suggesting that some species play a keystone role in winter foraging flocks. More generally, these analyses demonstrate that this method provides a powerful approach, using social networks to quantify the relative transmission rates across different social relationships.
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The ability to adjust behavioral responses to environmental cues probably contributes to an individual's ability to persist in unfamiliar habitats. One behavior, how an individual responds to novelty, influences the acquisition of resources (e.g., novel foods) and identification of stressors, but it may also increase exposure to risks. Here, using house sparrows (Passer domesticus) recently introduced to Kenya, we tested how range expansion influenced individuals' responses to novel foods and objects. We predicted that range edge birds would be less averse to novelty than birds at the site of introduction and that this effect would be more pronounced for novel foods than novel non-nutritional items. We also expected range edge individuals to be more sensitive to changes in the environment and therefore more apt to adjust their behavior in response to different cues; in other words, individuals at the range edge would have a more flexible behavioral repertoire than individuals at the site of introduction. As predicted, individuals at the range edge ate novel foods faster than those from established areas; however, latency to touch novel objects did not vary across the range. Individuals throughout the range were variable in their response to novelty, but there was no indication that individual flexibility was greater at the range edge. Although many novel items might be useful to introduced organisms, novel foods are likely more valuable, and therefore individuals should be most apt to risk the potential costs associated with novelty for a high nutritional payoff.
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Resident and nomadic species differ substantially in their mobility, with the former spending most of their lives in a restricted area and the latter encountering many areas while tracking spatiotemporal unpredictable resources. Earlier studies have shown that information gathering differs alongside this mobility axis-resident species pay more attention to changes in their familiar environment than nomadic ones. However, little is known about spatial exploration in resident and nomadic species. We investigated spatial exploration in 10 closely related parrot species that differed in their mobility by giving them access to two unfamiliar aviaries left and right of the familiar aviary. For analyses, mobility and some diet and habitat variables were related to spatial exploration. Nomadic species spent less time exploring the novel aviaries and also started tactile exploration later than resident/nomadic and pure resident species. Furthermore, diet specialists visited more new locations in relation to their overall movements than diet generalists. The variables were not correlated with the molecular phylogeny (mitochondrial cytochrome b) of the species. The results indicate that nomads invest less in spatial exploration than residents possibly because they stay only for limited periods of time in one particular area or use easier-to-assess cues. Residents, in contrast, assess a novel environment in detail as they may collect information about future breeding sites for which they need short-and long-term information. Finally, diet specialists may pay attention to fewer environmental cues than generalists, which allows them to move faster through a novel environment.
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True bugs are generally considered to be well protected against bird predation. Sympatric species that have similar warning coloration are supposed to form a functional Müllerian mimetic complex avoided by visually oriented avian predators. We have tested whether these assumptions hold true for four species of European red-and-black heteropterans, viz. Pyrrhocoris apterus, Lygaeus equestris, Spilostethus saxatilis, and Graphosoma lineatum. We found that individual species of passerine birds differ in their responses towards particular bug species. Great tits (Parus major) avoided all of them on sight, robins (Erithacus rubecula) and yellowhammers (Emberiza citrinella) discriminated among them and attacked bugs of some species with higher probability than others, and blackbirds (Turdus merula) frequently attacked bugs of all the tested species. Different predators thus perceive aposematic prey differently, and the extent of Batesian-Müllerian mimetic complexes and relations among the species involved is predator dependent.
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Insect communities consist of aposematic species with efficient warning colours against predation, as well as abundant examples of crypsis. To understand such coexistence, we here report results from a field experiment where relative survival of artificial larvae, varying in conspicuousness, was estimated in natural bird communities over an entire season. This takes advantage of natural variation in the proportion of naive predators: naivety peaks when young birds have just fledged. We show that the relative benefit of warning signals and crypsis changes accordingly. When naive birds are rare (early and late in the season), conspicuous warning signals improve survival, but conspicuousness becomes a disadvantage near the fledging time of birds. Such temporal structuring of predator-prey relationships facilitates the coexistence of diverse antipredatory strategies and helps explain two patterns we found in a 688-species community of Lepidoterans: larval warning signals remain rare and occur disproportionately often in seasons when predators are educated.
The book discusses the diversity of mechanisms by which prey can avoid or survive attacks by predators, both from ecological and evolutionary perspectives. There is a particular focus on sensory mechanisms by which prey can avoid being detected, avoid being identified, signal (perhaps sometimes dishonestly) to predators that they are defended or unpalatable. The book is divided into three sections. The first considers detection avoidance through, for example, background matching, disruptive patterning, countershading and counterillumination, or transparency and reflective silvering. The second section considers avoiding or surviving an attack if detection and identification by the predator has already taken place (i.e., secondary defences). The key mechanism of this section is aposematism: signals that warn the predator that a particular prey type is defended. One particularly interesting aspect of this is the sharing of the same signal by more than one defended species (the phenomenon of Mullerian mimicry). The final section considers deception of predators. This may involve an undefended prey mimicking a defended species (Batesian mimicry), or signals that deflect predator’s attention or signals that startle predators. The book provides the first comprehensive survey of adaptive coloration in a predator-prey context in thirty years.
Aggregations in insects carry out diverse functions, and gregariousness may also act as an antipredatory strategy, especially when combined with warning signalling. Despite many studies focused on the antipredatory function of gregariousness, there are still aspects needing further investigation: What aspects of predator behaviour are affected by prey gregariousness? Which of the antipredatory effects of aggregations are linked with aposematic coloration, and which will also work for non-aposematic prey? Does gregariousness of an aposematic species affect its mimetic relationships? We have studied these topics in the firebug, Pyrrhocoris apterus (Heteroptera), an aposematic red-and-black true bug with moderate chemical defence. Firebugs alternate between solitary and gregarious lifestyles throughout the year. We used hand-reared great tits (Parus major) as naive predators, and subjected them to avoidance training with either solitarily or gregariously presented firebugs, followed by a memory test with solitary individuals. To test whether effects of gregariousness are specific for the aposematic firebugs, we tested another group of birds with brown-painted firebugs. Our results show that the gregarious lifestyle of the firebug is a part of its antipredatory strategy. Compared to solitary individuals, aggregations benefited in several ways, some exclusive for aposematic firebugs, others working irrespective of coloration. Aggregations induced greater innate wariness, leading to longer attack latencies and more cautious prey handling, including complete attack avoidance in some birds. Despite the fact that the birds mostly attacked only one or two individuals from an aggregation, they needed fewer trials to reach the avoidance-learning criterion than the birds learning to avoid solitary firebugs. Birds’ experience with firebug aggregations reduced the predation risk of subsequently encountered solitary individuals, as the birds hesitated longer before attacking a solitary firebug if their previous aversive experience had been with aggregations rather than with solitary individuals. Predators’ experience with firebug aggregations may compensate for the firebugs’ moderate chemical defence, and as a consequence, gregariousness may change the firebugs’ mimetic relationships with better defended red-and-black true bug species from quasi-Batesian to Müllerian.
Colour polymorphism is a widespread phenomenon in vertebrates and has often been linked with differences in behaviour such as aggression or boldness, behaviours that are often part of personality traits in monomorphic species. However, up to now, very few studies have looked whether colour morphs just differ in average behaviour or whether specific combinations of behaviours are favoured in relation to a particular morph therefore signalling personality traits. This was tested in the highly social and polymorphic Gouldian finch (Erythrura gouldiae). Tests were performed in pairs of a red-headed and a black-headed individual of same sex and size but different age. Capture rank in the aviary as well as latency to feed beside a novel object (neophobia) and to approach and touch a novel object on a perch (neophilia) were measured. For neophobia and neophilia, ranks of latencies calculated across all individuals were used and general and within-pair comparisons were made. Neophobia and approach neophilia were consistent over time (2 mo), and approach neophilia was positively correlated with capture rank and neophobia indicating that the behaviours are part of personality traits. Moreover, black-headed birds generally approached the novel object earlier than red-headed birds. Similarly, within pairs, black-headed birds were first to approach the novel object and were also captured first. Relative age (younger or older than the partner) was related to neophobia and tactile neophilia ranks; older birds reacted faster. The results indicate that colour morphs not only differ in average behaviour but that specific combinations of behaviours are related to colour morphs suggesting that head colours signal personality traits. Furthermore, depending on age individuals may have different roles in a social network.