Different reactions to aposematic prey in 2 geographically distant populations of great tits

Abstract

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.

Full text

© The Author 2015. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved. For
permissions, please e-mail: journals.permissions@oup.com
The ocial journal of the
ISBE
International Society for Behavioral Ecology
Behavioral
Ecology
Original Article
Dierent reactions to aposematic prey in
2 geographically distant populations of
greattits
AliceExnerová,
a
DanaJežová,
a
PavelŠtys,
a
LuciaDoktorovová,
a
BibianaRojas,
b
and JohannaMappes
b
a
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 43 Praha
2, Czech Republic and
b
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.
INTRODUCTION
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: exnerova@gmail.com.
Behavioral Ecology (2015), 00(00), 1–10. doi:10.1093/beheco/arv086
Behavioral Ecology Advance Access published June 25, 2015
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

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.
MATERIALS AND METHODS
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
Finland
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°38′N),
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).
Predators
Altogether we tested 100 wild-caught great tits, 50 from each of 2
geographically distant populations: 1)Konnevesi in Central Finland
(62°38′N, 26°19′E) and 2) Prague in Bohemia (Czech Republic,
50°04′N, 14°26′E). 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
Page 2 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

Exnerová et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.
Prey
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
libitum.
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
latency.
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.
Page 3 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

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.
Firebugtest
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
themodel.
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.
RESULTS
Comparison of occurrence of aposematic species
of Heteroptera in Central Europe and Central
Finland
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
P=0.006).
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).
Page 4 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

Exnerová et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
s
=0.60, t=5.15, df=48, and P<0.05; Bohemian birds:
r
s
=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
s
 = 0.04, t = 0.27, df = 48, NS;
Bohemian birds: r
s
=0.02, t=0.12, df=48, NS) and neophobia
(Finnish birds: r
s
= 0.06, t=0.40, df= 48, NS; Bohemian birds:
r
s
=0.16, t=1.10, df=48, NS) tests.
Reaction to aposematic and nonaposematic
firebugs
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
P=0.004).
Table1
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*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.
500
400
300
200
Central Finland Bohemia
Exploration test
Neophobia test
Latency (s) (Mean +/- SE)
100
0
Figure1
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
bars).
Table2
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).
3000
2500
2000
1500
1000
500
0
Blue cricket
Nonaposematic firebug
Aposematic firebug
Latency to attack (s) (Mean +/- SE)
Central Finland Bohemia
Figure2
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).
Page 5 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

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
s
=0.46, t=2.46, df=23,
and P < 0.05; nonaposematic bugs: r
s
=0.61, t=3.65, df=23, and
P<0.05); for Bohemian birds no such correlation was found (apo-
sematic bugs: r
s
=0.10, t=0.49, df=23, NS; nonaposematic bugs:
r
s
=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).
DISCUSSION
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
Table4
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
None
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.
1.8
1.5
1.2
0.9
0.6
0.3
0.0
Central Finland Bohemia
Nonaposematic
Aposematic
Number of firebugs attacked (Mean + SE)
Figure3
Dierence between Bohemian and Central Finnish great tits in the number
of nonaposematic and aposematic firebugs attacked.
Table5
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.
Table3
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.
Page 6 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

Exnerová et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
habitats.
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
dangerousprey.
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
firebugs
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
Page 7 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

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).
CONCLUSIONS
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.
FUNDING
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
Page 8 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

Exnerová etal. • Geographic dierences in behavior toward aposematicprey
REFERENCES
An YS, Kriengwatana B, Newman AE, MacDougall-Shackleton EA,
MacDougall-Shackleton SA. 2011. Social rank, neophobia and observa-
tional learning in black-capped chickadees. Behaviour. 148:55–69.
Aronsson M, Gamberale-Stille G. 2008. Domestic chicks primarily attend
to colour, not pattern, when learning an aposematic coloration. Anim
Behav. 75:417–423.
Aukema B, Rieger C. 2001. Catalogue of the Heteroptera of the Palaearctic
region. Vol. 4. Amsterdam (The Netherlands): The Netherlands
Entomological Society.
Barnett CA, Bateson M, Rowe C. 2007. State-dependent decision making:
educated predators strategically trade o the costs and benefits of con-
suming aposematic prey. Behav Ecol. 18:645–651.
Barnett CA, Skelhorn J, Bateson M, Rowe C. 2012. Educated predators
make strategic decisions to eat defended prey according to their toxin
content. Behav Ecol. 23:418–424.
Bell AM. 2005. Behavioural dierences between individuals and two popu-
lations of stickleback (Gasterosteus aculeatus). J Evol Biol. 18:464–473.
Bókony V, Kulcsár A, Tóth Z, Liker A. 2012. Personality traits and behav-
ioral syndromes in dierently urbanized populations of house sparrows
(Passer domesticus). PLoS One. 7:e36639.
Brower LP. 1988. Avian predation on the monarch butterfly and its implica-
tions for mimicry theory. Am Nat. S4–S6.
Brydges NM, Colegrave N, Heathcote RJ, Braithwaite VA. 2008. Habitat
stability and predation pressure aect temperament behaviours in popu-
lations of three-spined sticklebacks. J Anim Ecol. 77:229–235.
Cepák J, Klvaňa P, Škopek J, Schröpfer L, Jelínek M, Hořák D, Formánek
J, Zárybnický. 2008. Bird Migration Atlas of the Czech Republic and
Slovakia. Praha (Czech Republic): Aventinum.
Coppinger RP. 1969. The eect of experience and novelty on avian feeding
behaviour with reference to the evolution of warning colouration in but-
terflies. Part I: Reactions of wild-caught adult blue jays to novel insects.
Behaviour. 35:45–60.
Coppinger RP. 1970. The eect of experience and novelty on avian feeding
behavior with reference to the evolution of warning coloration in butter-
flies. II. Reactions of naive birds to novel insects. Am Nat. 104:323–335.
Cramp S, Perrins CM. 1993. The birds of Western Palearctic. Vol. 7.
Oxford (UK): Oxford University Press.
Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N.
2007. Behavioural syndromes dier predictably between 12 populations
of three-spined stickleback. J Anim Ecol. 76:1128–1138.
Drent PJ, van Oers K, van Noordwijk AJ. 2003. Realized heritability of
personalities in the great tit (Parus major). Proc R Soc B. 270:45–51.
Echeverría AI, Vassallo AI. 2008. Novelty responses in a bird assemblage
inhabiting an urban area. Ethology 114: 616–624.
Endler JA, Mappes J. 2004. Predator mixes and the conspicuousness of
aposematic signals. Am Nat. 163:532–547.
Evans J, Boudreau K, Hyman J. 2010. Behavioural syndromes in urban and
rural populations of song sparrows. Ethology. 116:588–595.
Exnerová A, Hotová Svádová K, Fučíková E, Drent P, Štys P. 2010.
Personality matters: individual variation in reactions of naive bird preda-
tors to aposematic prey. Proc R Soc B. 277:723–728.
Exnerová A, Landová E, Štys P, Fuchs R, Prokopová M, Cehláriková P.
2003. Reactions of passerine birds to aposematic and nonaposematic fire-
bugs (Pyrrhocoris apterus; Heteroptera). Biol J Linn Soc. 78:517–525.
Exnerová A, Svádová K, Štys P, Barcalová S, Landová E, Prokopová M,
Fuchs R, Socha R. 2006. Importance of colour in the reaction of passer-
ine predators to aposematic prey: experiments with mutants of Pyrrhocoris
apterus (Heteroptera). Biol J Linn Soc. 88:143–153.
Exnerová A, Štys P, Fučíková E, Veselá S, Svádová K, Prokopová M,
Jarošík V, Fuchs R, Landová E. 2007. Avoidance of aposematic prey in
European tits (Paridae): learned or innate? Behav Ecol. 18:148–156.
Fabricant SA, Exnerová A, Ježová D, Štys P. 2014. Scared by shiny? The
value of iridescence in aposematic signalling of the hibiscus harlequin
bug. Anim Behav. 90:315–325.
Farine JP, Bonnard O, Brossut R, Le Quere JL. 1992. Chemistry of
defensive secretions in nymphs and adults of fire bug, Pyrrhocoris apterus
L.(Heteroptera, Pyrrhocoridae). J Chem Ecol. 18:1673–1682.
Farine DR, Aplin LM, Sheldon BC, Hoppitt W. 2015. Interspecific social
networks promote information transmission in wild songbirds. Proc R
Soc B. 282:20142804.
Feenders G, Klaus K, Bateson M. 2011. Fear and exploration in European
starlings (Sturnus vulgaris): a comparison of hand-reared and wild-caught
birds. PLoS One. 6:e19074.
Gamberale-Stille G, Tullberg BS. 1999. Experienced chicks show biased
avoidance of stronger signals: an experiment with natural colour varia-
tion in live aposematic prey. Evol Ecol. 13:579–589.
Greenberg R. 1989. Neophobia, aversion to open space, and ecological
plasticity in song and swamp sparrows. Can J Zool. 67:1194–1199.
Greenberg R, Mettke-Hofmann C. 2001. Ecological aspects of neophobia
and neophilia in birds. Curr Ornithol. 16:119–178.
Halpin CG, Skelhorn J, Rowe C. 2014. Increased predation of nutrient-
enriched aposematic prey. Proc R Soc B. 281:20133255.
Ham A, Ihalainen E, Lindström L, Mappes J. 2006. Does colour matter?
The importance of colour in avoidance learning, memorability and gen-
eralisation. Behav Ecol Sociobiol. 60:482–491.
Hart NS. 2001. Variations in cone photoreceptor abundance and the visual
ecology of birds. J Comp Physiol A. 187:685–697.
Hotová Svádová K, Exnerová A, Kopečková M, Štys P. 2010. Predator
dependent mimetic complexes: do passerine birds avoid Central
European red-and-black Heteroptera? Eur J Entomol. 107:349–355.
Hotová Svádová K, Exnerová A, Kopečková M, Štys P. 2013. How do
predators learn to recognize a mimetic complex: experiments with naïve
great tits and aposematic Heteroptera. Ethology. 119:814–830.
Hotová Svádová K, Exnerová A, Štys P. 2014. Gregariousness as a defence
strategy of moderately defended prey: experiments with Pyrrhocoris apterus
and avian predators. Behaviour. 151:1617–1640.
Ihalainen E, Lindström L, Mappes J, Puolakkainen S. 2008. Can experi-
enced birds select for Müllerian mimicry? Behav Ecol. 19:362–368.
Korsten P, Mueller JC, Hermannstädter C, Bouwman KM, Dingemanse NJ,
Drent PJ, Liedvogel M, Matthysen E, van Oers K, van Overveld T, etal.
2010. Association between DRD4 gene polymorphism and personality vari-
ation in great tits: a test across four wild populations. Mol Ecol. 19:832–843.
Kristenová M, Exnerová A, Štys P. 2011. Seed preferences of Pyrrhocoris
apterus (Heteroptera: Pyrrhocoridae): are there specialized trophic popula-
tions? Eur J Entomol. 108:581–586.
Langham GM. 2006. Rufous-tailed jacamars and aposematic butterflies: do
older birds attack novel prey? Behav Ecol. 17:285–290.
Liebl AL, Martin LB, 2014. Living on the edge: range edge birds consume
novel foods sooner than established ones. Behav Ecol. 25:1089–1096.
Lindström L, Alatalo RV, Mappes J. 1999a. Reactions of hand-reared and
wild-caught predators toward warningly colored, gregarious, and con-
spicuous prey. Behav Ecol. 10:317–322.
Lindström L, Alatalo RV, Mappes J, Riipi M, Vertainen L. 1999b. Can apo-
sematic signals evolve by gradual change? Nature. 397:249–251.
Lindström L, Rowe C, Guilford T. 2001. Pyrazine odour makes visually
conspicuous prey aversive. Proc R Soc B. 268:159–162.
Mappes J, Alatalo RV. 1997. Eects of novelty and gregariousness in sur-
vival of aposematic prey. Behav Ecol. 8(2):174–177.
Mappes J, Kokko H, Ojala K, Lindström L. 2014. Seasonal changes in
predator community switch the direction of selection for anti-predatory
defences. Nat Commun. 5:5016.
Marples NM, Kelly DJ. 1999. Neophobia and dietary conservatism: two
distinct processes? Evol Ecol. 13:641–653.
Marples NM, Mappes J. 2011. Can the dietary conservatism of predators
compensate for positive frequency dependent selection against rare, con-
spicuous prey? Evol Ecol. 25:737–749.
Marples NM, Roper TJ. 1996. Eects of novel colour and smell on
the response of naive chicks towards food and water. Anim Behav.
51:1417–1424.
Marples NM, Roper TJ, Harper DGC. 1998. Responses of wild birds to
novel prey: evidence of dietary conservatism. Oikos. 83:161–165.
Martin LB, Fitzgerald L. 2005. A taste for novelty in invading house spar-
rows, Passer domesticus. Behav Ecol. 16:702–707.
Mastrota NF, Mench JA. 1994. Avoidance of dyed food by the northern
bobwhite. Appl Anim Behav Sci. 42:109–119.
Mastrota NF, Mench JA. 1995. Colour avoidance in northern bobwhites:
eects of age, sex and previous experience. Anim Behav. 50:519–526.
Mettke-Hofmann C. 2012. Head colour and age relate to personality traits
in gouldian finches. Ethology. 118:906–916.
Mettke-Hofmann C, Lorentzen S, Schlicht E, Schneider J, Werner F. 2009.
Spatial neophilia and spatial neophobia in resident and migratory war-
blers (Sylvia). Ethology. 115:482–492.
Mettke-Hofmann C, Wink M, Braun M, Winkler H. 2012. Residency and
a broad feeding spectrum are related to extensive spatial exploration in
parrots. Behav Ecol. 23:1365–1371.
Mettke-Hofmann C, Winkler H, Hamel PB, Greenberg R. 2013. Migratory
New World blackbirds (icterids) are more neophobic than closely related
resident icterids. PLoS One. 8:e57565.
Page 9 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from

Behavioral Ecology
Mettke-Hofmann C, Winkler H, Leisler B. 2002. The significance of
ecological factors for exploration and neophobia in parrots. Ethology.
108:249–272.
Miranda AC, Schielzeth H, Sonntag T, Partecke J. 2013. Urbanization and
its eects on personality traits: a result of microevolution or phenotypic
plasticity? Glob Change Biol. 19:2634–2644.
Nokelainen O, Valkonen J, Lindstedt C, Mappes J. 2014. Changes in preda-
tor community structure shifts the ecacy of two warning signals in
Arctiid moths. J Anim Ecol. 83: 598–605.
Rintala T, Rinne V. 2010. Suomen Luteet. Helsinki (Finland):
Hyönteistarvike Tibiale Oy.
Roper T, Redston S. 1987. Conspicuousness of distasteful prey aects the
strength and durability of one-trial avoidance learning. Anim Behav.
35:739–747.
Rowe C, Guilford T. 1996. Hidden colour aversions in domestic chicks
triggered by pyrazine odours of insect warning displays. Nature.
383:520–522.
Ruxton GD, Sherratt TN, Speed MP. 2004. Avoiding atack. The evolution of
crypsis, warning signals and mimicry. New York: Oxford University Press.
Schuh RT, Slater JA. 1995. True bugs of the world (Hemiptera:
Heteroptera): classification and natural history. Ithaca and London (USA
and UK): Cornell University Press.
Sillén-Tullberg B. 1985. Higher survival of an aposematic than of a cryptic
form of a distasteful bug. Oecologia. 67:411–415.
Shochat E, Lerman SB, Katti M, Lewis DB. 2004. Linking optimal foraging
behavior to bird community structure in an urban-desert landscape: field
experiments with artificial food patches. Am Nat. 164:232–243.
Smith SM. 1975. Innate recognition of coral snake pattern by a possible
avian predator. Science. 187:759–760.
Sol D, Lefebvre L, Rodríguez-Teijeiro JD. 2005. Brain size, innovative pro-
pensity and migratory behaviour in temperate Palaearctic birds. Proc R
Soc B. 272:1433–1441.
Speed MP. 2000. Warning signals, receiver psychology and predator mem-
ory. Anim Behav. 60:269–278.
Svádová K, Exnerová A, Štys P, Landová E, Valenta J, Fučíková A, Valenta
J, Socha R. 2009. Role of dierent colours of aposematic insects in learn-
ing, memory and generalization of naive bird predators. Anim Behav.
77:327–336.
Tebbich S, Fessl B, Blomqvist D. 2009. Exploration and ecology in Darwin´s
finches. Evol Ecol. 23:591–605.
Valkonen JK, Nokelainen O, Niskanen M, Kilpimaa J, Björklund M,
Mappes J. 2012. Variation in predator species abundance can cause
variable selection pressure on warning signaling prey. Ecol Evol.
2:1971–1976.
van Oers K, Drent P, de Jong G, van Noordwijk A. 2004. Additive and
nonadditive genetic variation in avian personality traits. Heredity.
93:496–503.
Verbeek ME, Drent PJ, Wiepkema PR. 1994. Consistent individual dif-
ferences in early exploratory behaviour of male great tits. Anim Behav.
48:1113–1121.
Wachmann E, Melber A, Deckert J. 2004. Wanzen 2. Die Tierwelt
Deutschlands 75. Keltern (Germany): Goecke & Evers.
Wachmann E, Melber A, Deckert J. 2006. Wanzen 1. Die Tierwelt
Deutschlands 77. Keltern (Germany): Goecke & Evers.
Wachmann E, Melber A, Deckert J. 2007. Wanzen 3. Die Tierwelt
Deutschlands 78. Keltern (Germany): Goecke & Evers.
Wachmann E, Melber A, Deckert J. 2008. Wanzen 4. Die Tierwelt
Deutschlands 81. Keltern (Germany): Goecke & Evers.
Page 10 of 10
at Jyvaskylan Yliopisto on June 26, 2015http://beheco.oxfordjournals.org/Downloaded from