Ethology 108, 429—441 (2002)

2002 Blackwell Verlag, Berlin

ISSN 0179–1613

An Experimental Study of Predator Recognition in Great Tit

Fledglings

Cecilia Kullberg* & Johan Lind

*Ornithology Group, Division of Environmental & Evolutionary Biology, Institute of
Biomedical and Life Sciences, Glasgow University, Glasgow, UK; Department of
Zoology, Stockholm University, Stockholm, Sweden

Abstract
Studies of naturally predator-naı̈ve adult birds (finches on predator-free
islands) and birds experimentally hand reared in isolation from predators indicate
that birds can recognise predators innately; that is, birds show anti-predator
behaviour without former experience of predators. To reduce predation risk
efficiently during the vulnerable fledgling period, we would predict an innate
response to be fully developed when the chicks leave the nest. However, 30-day-
old naı̈ve great tit fledglings (Parus major) did not respond differently to a model
of a perched predator than to a similarly sized model of a non-predator. Although
chicks showed distress responses such as warning calls and freezing behaviour,
they did not differentiate between the stimuli. In contrast, wild-caught first-year
birds (4 mo old) and adults responded differentially to the two stimuli. Lack of
recognition of a perched predator might be one explanation for the high mortality
rate found in newly fledged great tits. Our results imply that parental care is not
only important for food provisioning, but also to reduce predation risk during the
time when fledglings are most vulnerable.
Corresponding author: C. Kullberg, Tovetorp Research Station, Stockholm
University, SE-640 50 Björnlunda, Sweden. E-mail: cecilia.kullberg@zoologi.
su.se

Introduction
Because the failure to escape a predator causes death to a prey animal, and
thus excludes opportunities to reproduce in the future, predation is a major
selective force in nature (e.g. Dawkins & Krebs 1979). There is thus strong selection
for both morphological characters and behaviours that reduce the risk of a prey
being caught by a predator (Lima & Dill 1990). When prey detect a predator, they
often alter their behaviour to reduce the risk of being caught, by escaping, staying
motionless or by showing some other anti-predator behaviour, for example.

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430 C. Kullberg & J. Lind

However, to be able to do this, the prey must be able to identify predators and
distinguish them from non-dangerous animals (McLean & Rhodes 1991; Curio
1993). A question not readily answered is whether this ability is innate or if it has to
be fully or partially acquired through learning. Several different nonexclusive
possibilities of how animals acquire predator recognition have been suggested:
animals may have a genetically programmed ability to recognize predators without
earlier experience with that very predator, or they may be sensitised to learn about
particular stimuli very quickly. There may also be age-related maturation of the
ability to express a recognition response. Furthermore, learning about dangerous
predators through cultural transmission and teaching has been shown to exist in
many animals (Curio et al. 1978; Hirsch & Bolles 1980; Johnston 1982; McLean
& Rhodes 1991; Caro & Hauser 1992; Curio 1993; Maloney & McLean 1995;
Mathis et al. 1996). One of the first experiments suggested that ducks and geese
have an innate ability to recognize a flying hawk from a flying goose (Tinbergen
1951). However, the interpretation of Tinbergen’s results has been questioned since
the birds under study were reared in a natural environment in which they may have
been more habituated to geese than to hawks (Schleidt 1961a, b in Curio 1993;
Gray 1987; but see Canty & Gould 1995). Subsequent studies on spiders, fish and
mammals have shown clear evidence for an innate component to predator
recognition. The most convincing evidence derives from studies reporting genetic
differences in predator response in naı̈ve individuals from different populations
with varying predation risk (an American funnel building spider, Agelenopsis
aperta, Riechert & Hedrick 1990; guppy, Poecilia reticulata, Seghers 1974; three-
spined stickleback, Gasterosteus aculeatus, Tulley & Huntingford 1987; European
minnow, Phoxinus phoxinus, Magurran 1990; California ground-squirrel, Spermo-
philus beecheyi, Owings & Coss 1977; deermouse, Peromyscus maniculatus, Hirsch
& Bolles 1980). Furthermore, naturally predator-naı̈ve finches (Geospiza sp.) on a
predator-free island (Curio 1969), and zebra finches, Taeniopygia guttata, reared in
captivity for several generations (Lombardi & Curio 1985) can distinguish between
predators and non-dangerous animals.
Juvenile altricial birds typically face a high predation risk during their first
period outside the nest, because of their inexperience in flight and other
behaviours (Perrins 1979). Some predators, such as the sparrowhawk, seem to
have a preference for fledglings as food for their own chicks (Perrins & Geer 1980;
Geer 1981; Newton & Marquiss 1982). A recent radio-telemetry study (Naef-
Daenzer et al. 1999) reported an extremely high daily mortality (32%), mainly
caused by predation, in fledgling great tits and coal tits, Parus ater, during the first
4 d outside the nest. After these 4 d the mortality quickly decreased to a level of
about 1% per day, which is nevertheless still higher than the adult mortality of
0.15% per day (see also Perrins & Geer 1980). To minimise predation risk in
fledglings when they leave the nest and are likely to meet a predator for the first
time, we would expect an innate response to predators to be fully developed.
There are two published studies on the ability of truly naı̈ve fledgling birds to
recognise predators (Hinde 1954; Curio 1975). Both these studies indicate that the
ability to recognize predators is innate and develops in the chicks in the absence of
 Predator Recognition in Birds 431
their parents. Furthermore, Curio suggests that predator recognition is non-
existent in naı̈ve fledglings, but develops as chicks grow older. Here we present a
study of predator recognition in hand-reared great tit fledglings, Parus major. In
order to shed light on the ability of predator recognition in very young fledglings
we chose to study the responses of fledglings at an age when they normally still
receive parental care.

Methods
Subjects and Husbandry

One-week-old great tit nestlings were collected from nest boxes in the area
around Tovetorp Zoological Research Station (90 km south of Stockholm,
5856¢ N 1708¢ E) in June 1999. The nestlings were held in wooden boxes
together with their siblings at Tovetorp and hand-raised until they fledged and
could feed by themselves (about 3 wks of age). The nestlings were fed with
commercial canned dog food supplemented with water, vitamins, calcium, boiled
eggs, maggots (Calliphora sp.), and mealworms (Tenebrio molitor). When the
birds fledged they also had access to sunflower seeds, hemp seeds, suet and water
ad libitum. About five birds, with individual colour bands, were kept in each of
four holding rooms (1.75 m · 2.40 m · 1.95 m high). In each holding room there
was an artificial Christmas tree, a small birch tree without leaves and additional
perches along the walls. The rooms were lit by daylight fluorescent tubes
following the natural outdoor day length. Wild great tits were caught at the end of
Sep. 1999. Birds were aged by the colour of their wing coverts (Svensson 1992). In
total, 16 wild first-year great tits (seven females and nine males) and 14 wild adult
great tits (five females and nine males) were exposed to exactly the same
experiments as the naı̈ve birds had been. The wild birds were kept in the same
holding rooms where the naı̈ve birds had been.

Behavioural Screening
In order to study predator recognition in the naı̈ve great tits they were
subjected to presentations of a stuffed perched sparrowhawk (Accipiter nisus) and,
as a control, a stuffed perched grey partridge (Perdix perdix). Both species occur
sympatrically with great tits, the sparrowhawk being a raptor preying upon small
birds, while the partridge is vegetarian. The partridge was chosen as control
species to rule out size effects (total length: sparrowhawk, 28–38 cm; partridge,
29–31 cm; Jonsson 1992). The experiments started when the great tits were
approximately 4 wks of age. At this age they were feeding by themselves and
reacted to their human tenders by escaping when we tried to catch them.
However, because parental care continues for about 20 d after fledging in great
tits (Cramp & Perrins 1993; Verhulst & Hut 1996) they were at an age when they
would still be tended for by their parents.
432 C. Kullberg & J. Lind

The birds were tested individually in an experimental room

(2.40 m · 1.20 m · 1.95 m high) similar to the holding room (Fig. 1). In one
side of the room there was protective cover consisting of branches from an
artificial Christmas tree. From this cover, a perch with a feeding tray filled with
mealworms was extended. On the other side of the room, the stuffed bird could be
made visible by pulling it up from a covered plastic tube by an arrangement from
outside the room. Between the plastic tube and the cover there were two poles (A
and B) with several perches (Fig. 1). All four walls were solid and the behaviour of
the great tits was recorded by a DVD video camera through a hole in one wall. In
total, 20 naı̈ve great tits were used in the experiments. Eleven of the birds were
exposed to the sparrowhawk on the 1st day and to the partridge on the next day
(referred to as ‘1st hawk’ in the results). The other nine birds were exposed to the
two stuffed models in reversed order (referred to as ‘1st partridge’ in the results).
In order to control the feeding motivation of the birds, individuals were kept in a
holding bag made of cloth for a maximum of 1 h before the experiment. We chose
this method rather than putting the bird into an individual cage because the
juveniles were not used to being alone in a cage, and would thus probably be more
stressed than in a dark place resembling a nesting hole. After 1 h the bird was
released into the experimental room and the stuffed bird (either sparrowhawk or
partridge depending on the experimental schedule) was pulled up from the plastic
tube as soon as the bird took a mealworm from the feeding tray. The time from
when the bird was released until it started to feed ranged between 5 and 15 min.
The stuffed bird was exposed for 5 min before it disappeared into the plastic tube
again.
The behaviour of the birds during the exposure to the stuffed birds was
recorded by analysing the video. The following behaviours were recorded.

Fig. 1: The experimental set-up. The stuffed bird could be made visible by pulling it up from a plastic
tube. There were two perches between the shelter with the feeding tray and the stuffed bird: perch A
and perch B
 Predator Recognition in Birds 433
• Main activity during each minute of the 5-min exposure period, cate-
gorised as one of the following categories:
Freezing: not moving any part of the body.
Sitting still: only slow and careful movements of the body.
Normal activity: moving around without signs of distress, sometimes eating.
Distressed: quick jerky movements, bobbing of head, wing flicking often
together with warning calls (described as mobbing behaviour by Hinde 1952).
• Number of movements between perches during each of the 5 min.
• Time until the first feeding event after the stuffed bird was made visible. If
the bird did not eat during the 5 min the stuffed bird was visible, we recorded for a
further 5 min after the stuffed bird had disappeared. A bird that did not eat
during this time was given the maximum time of 600 s.
• Number of warning calls (called ‘scolding’ by Hinde 1952) during each of
the 5 min.
• Time until the great tit approached the stuffed bird by moving to one of
the two perches A or B (see Fig. 1). If the bird did not use the perch A or B when
the stuffed bird was visible it was given the maximum time of 300 s.
When all of the naı̈ve great tits had been subjected to both experimental
treatments (sparrowhawk and partridge) the birds were held in an outdoor aviary
for 2 wks before they were released into the wild.
Before exposing the wild great tits to the experiment, we allowed them to
acclimatise for at least 2 d in their new environment. During this period the wild
birds ate readily. In each age category, half of the birds were shown the
sparrowhawk on the 1st day and the partridge on the subsequent day (referred to
as ‘1st hawk’ in the results). The other half was exposed to the two stuffed models in
reversed order (referred to as ‘1st partridge’ in the results). The behaviours were
analysed from the video in the same way as for the naı̈ve birds, but we also recorded
the activity during 1 min after the stuffed bird had disappeared (categorised as
freezing, sitting still, normal activity, distressed). When each wild bird had been
exposed to both experimental treatments, it was released into the wild.

Statistical Analyses
We used Mann–Whitney U-tests for continuous data, and Fisher’s exact test
and G-test (Zar 1999) for categorical data. Statistical calculations (except for
G-test which was calculated by hand) were made using STATISTICA for Windows
5.1, Statsoft Inc.

Results
Sequence Effects

Because each of the great tits was exposed to both of the two stuffed birds,
their reactions to the stimuli might be affected by the order in which they had been
434 C. Kullberg & J. Lind

presented. The naı̈ve birds moved more during the first minute of exposure and
approached the stuffed partridge faster if they had former experience of a
sparrowhawk in the experimental room than if it was their first experience in the
room (Mann–Whitney U-test; movements when exposed to partridge: U ¼ 9.5,
n1st partridge ¼ 9, n1st hawk ¼ 11, p < 0.01; time to approach to A: U ¼ 5.0,
n1st partridge ¼ 9; n1st hawk ¼ 11, p < 0.001, still being significant after sequential
Bonferroni correction, Rice 1989). The behaviours tested were: latency to feed;
number of warning calls; number of movements; and latency to approach perch A
and B, respectively. The other three measured behaviours were not significantly
different depending on the order of exposure. There was no difference in
behavioural reaction of the naı̈ve great tits to the stuffed sparrowhawk depending
on the order of exposure (Mann–Whitney U-test with sequential Bonferroni
correction for five subsequent tests for the different behaviours). Additionally,
among the wild great tits there were no significant differences in behavioural
reactions depending on the order of exposure (Mann–Whitney U-test with
sequential Bonferroni correction for five subsequent tests for the different
behaviours). However, because there is an effect of order of exposure on the
behaviour of naı̈ve birds, and above all, because the comparisons of behaviour
within and between groups of birds (naı̈ve and wild) give the same results, we have
chosen only to report statistics from the first experience of the experimental set-up
for each individual (both concerning wild and naı̈ve birds). As mentioned in the
Methods, we recorded behaviour of the great tits during each of the 5 min they
were exposed to the stuffed model. However, because all measurements gave
similar results for the subsequent minutes, we only report statistics for the first
minute of the exposure. Furthermore, because there were no differences between
wild first-year and adult great tits in any of the behaviours recorded, we pooled
the two age classes in the analysis.

Differences in Response to Hawk vs. Partridge

We could not find any significant differences in the responses between the
group of naı̈ve great tits exposed to the sparrowhawk and the group exposed to
the partridge (Fig. 2). The most common main activity during exposure to both of
the stuffed birds was normal activity. However, in response to both the
sparrowhawk and the partridge, some birds showed distress by quick jerky
movements, bobbing of head, wing flicking and emitting warning calls (Fig. 2).
Furthermore, there were no differences in the number of movements, number of
warning calls, time to first feeding event or time to approach the stuffed bird
between the group of naı̈ve birds exposed to the sparrowhawk and the group
exposed to the partridge (Figs 3 and 4).
In contrast to the naı̈ve great tits, the wild great tits showed distinct
differences in behaviour in response to the two stuffed birds. Wild birds exposed
to the sparrowhawk tended to show distress by quick jerky movements, bobbing
of head, wing flicking and emitting warning calls. However, most birds exposed to
the partridge showed normal activity without signs of distress (Fig. 2).
 Predator Recognition in Birds 435

Fig. 2: Percentage of naı̈ve and wild great tits showing different activities during the first minute of the
presentation of the partridge and the sparrowhawk. There was no difference in activity responses
between the group of naı̈ve great tits exposed to the sparrowhawk and the group exposed to the
partridge (G-test, G3 ¼ 5.01, p > 0.1). However, wild great tits showed differences in activity in
response to the two stuffed birds (G-test; G3 ¼ 12.2, p < 0.01, still being significant after a sequential
Bonferroni correction). There was no difference in activity response to either the partridge or the
sparrowhawk between naı̈ve and wild great tits (G-test, partridge: G3 ¼ 4.7, p > 0.1; sparrowhawk:
G3 ¼ 7.7; 0.1 > p > 0.05). Sample size is indicated above each bar

Furthermore, the group of birds exposed to the sparrowhawk moved less, emitted
more warning calls and waited longer until they resumed feeding than the group
exposed to the partridge (Fig. 3). Only two out of 15 wild birds exposed to the
sparrowhawk fed when it was present, whereas 13 of the 15 wild birds fed in the
presence of the stuffed partridge (Fishers exact test; p ¼ 0.02). Because we did not
see any special reactions by the naı̈ve great tits to the disappearance of the two
stuffed birds, we did not video-record during this period. However, when studying
wild birds later, we realised that there was a difference in activity patterns between
wild birds exposed to the hawk compared to wild birds exposed to the
partridge. Wild great tits that had been exposed to the sparrowhawk tended to
freeze for several minutes, while the great tits that had been exposed to the
partridge showed normal activity (Fig. 5).

Differences in Responses of Naı̈ve vs. Wild Birds

The only difference in response to the partridge between naı̈ve and wild great
tits was that wild birds moved more than naı̈ve birds (Table 1; Figs 2, 3 and 4).
However, there were clear differences between wild and naı̈ve birds in their
reactions to the sparrowhawk. Even though there was no significant difference in
activity between naı̈ve and wild birds, wild birds moved more, were less likely to
approach the sparrowhawk and waited longer until resuming feeding than naı̈ve
birds during sparrowhawk exposure (Table 1; Figs 2, 3 and 4). Wild birds were
436 C. Kullberg & J. Lind

Fig. 3: Number (median ± quartiles) of movements and warning calls during the first minute of the
presentation, and seconds until first feeding event, for naı̈ve and wild birds, respectively, during
presentation of the partridge and the sparrowhawk. The stuffed birds were removed after 300 s and the
maximum time we waited for the birds to start feeding was 600 s. Statistics from Mann–Whitney
U-test. Differences in number of movements, time until feeding, and number of warning calls in wild
birds are still significant after a sequential Bonferroni correction

less likely to eat during the sparrowhawk experiment (including the 5-min period
after the sparrowhawk had disappeared; three out of 15 birds) than naı̈ve birds
(10 out of 11 birds; Fishers exact test; p ¼ 0.001). We do not have any
quantitative data on the reaction of naı̈ve birds after the stimulus disappeared.
However, from our direct observations we could tell that there was a distinct
difference between wild and naı̈ve birds when the sparrowhawk disappeared, with
wild birds freezing for several minutes while no distinct behavioural changes were
seen in naı̈ve birds.

Discussion
The 30-day-old naı̈ve great tits showed various behaviours, such as distress
behaviour with warning calls and freezing behaviour, indicating that they were
physically capable of carrying out these behaviours. However, they appeared not
to discriminate between a harmless partridge and a predatory sparrowhawk. Even
though the birds were at an age when they would still be tended by their parents,
they were able to feed by themselves and their flight skills seemed well developed
(we could not catch them in their holding rooms without turning out the light).
 Predator Recognition in Birds 437

Fig. 4: Seconds (median ± quartiles) until the naı̈ve and wild birds, respectively, approached the two
perches A and B during presentation of the partridge and the sparrowhawk. Statistics from Mann–
Whitney U-test

Fig. 5: Percentage of wild birds showing different activities during the minute after the partridge and
the sparrowhawk, respectively, has disappeared. There was a difference in behavioural response after
the disappearance of the two stimuli (G-test, G3 ¼ 22.7, p < 0.001). Sample size is indicated above
each bar

Nevertheless, a flying raptor might elicit an inborn response, although an inborn

ability to discriminate between perched predators and harmless birds would also
be favourable, especially for inexperienced birds. Data on mortality in juvenile
438 C. Kullberg & J. Lind

Table 1: Comparison of the behaviours emitted by naı̈ve and wild great tits. Direction of
the difference between wild (W) and naı̈ve birds (N) is indicated for tests still being sig-
nificant after a sequential Bonferroni correction

Birds Behaviour Ua Pa Difference

Exposed to Partridgeb Number of movements 0 <0.001 W>N

Time until feeding 44.5 0.16
Number of warning calls 51.0 0.32
Approaching to perch A 39.5 0.09
Approaching to perch B 54.5 0.44
Exposed to Sparrowhawkc Number of movements 29.5 0.006 W>N
Time until feeding 21.5 0.002 W>N
Number of warning calls 37.0 0.02
Approaching to perch A 27.0 0.004 W>N
Approaching to perch B 37.5 0.02
a
Mann–Whitney U-test.
b
nnaı̈ve ¼ 9, nwild ¼ 15.
c
nnaı̈ve ¼ 11, nwild ¼ 15.

great tits suggests that they are heavily preyed upon when newly fledged (Naef-
Daenzer et al. 1999). Therefore, we think that to respond to perched predators is
relevant for the survival of inexperienced birds travelling in a new and unfamiliar
environment.
The reaction of wild caught first-year and adult great tits showed that, at
least for birds with experience in the wild, our experimental set up was sufficient to
elicit appropriate behaviour in response to the two stuffed birds. The wild birds
showed anti-predator behaviour when exposed to the sparrowhawk by emitting
warning calls and showing distress. Furthermore, compared to the wild birds
exposed to the stuffed partridge, they were much more reluctant to approach the
stuffed bird and to feed while it was still present. In addition, the wild birds
showed freezing behaviour after the sparrowhawk had disappeared. These
reactions to the stuffed sparrowhawk resemble reactions to avian predators in the
field (Ficken & Witkin 1977; Ficken 1990) and suggest that the wild birds
interpreted the stuffed sparrowhawk, but not the stuffed partridge, as a dangerous
predator.
It could be argued that an innate anti-predator response in 30-day-old
fledglings should be different from the response of older individuals (our wild
control birds were at least 4 mo old). Newly fledged birds are very vulnerable to
predation and we might expect an innate reaction to a perched sparrowhawk to
reduce the risk of detection. This should be in contrast to the reaction to perched
raptors of older and experienced great tits, which normally are characterised by
mobbing behaviour, actually making detection of the prey easier (Curio 1978).
However, the fledglings in this study did not seem to minimise predation risk
behaviourally by reducing the risk of detection or attack when exposed to the
 Predator Recognition in Birds 439
stuffed sparrowhawk. In fact they were more likely to approach the sparrowhawk,
and also more likely to eat in the presence of the sparrowhawk than were the wild
birds.
In a study by Tulley & Huntingford (1987), the importance of paternal care
for the development of innate anti-predator behaviour (without any earlier
experience of predators) in three-spined sticklebacks was convincingly shown.
Laboratory-raised predator-naı̈ve sticklebacks originating from a population
exposed to predatory pikes (Esox lucius) only showed appropriate avoidance
responses to a model pike if they had experienced paternal care. If they were
reared without their father they showed the same low response to the pike as
sticklebacks originating from a lake free from piscivorus fish.
As stated by Curio (1993), in all studies of animals reared in captivity
there is always a concern that the maturation of behaviour might be affected
by unnatural rearing conditions. The low anti-predator response in our naı̈ve
great tit fledglings might thus be explained by the absence of parents or
inadequacies in raising and/or housing, resulting in incomplete behavioural
development of an innate response. However, the fact that we observed both
freezing and distress behaviour in the naı̈ve birds indicates that they
developed these behaviours without the presence of parents. Furthermore,
we observed naı̈ve birds emitting ‘seet-calls’ in their holding rooms (without
any obvious reason) and individuals reacting to ‘seet-calls’ by freezing. Hinde
(1952) reported extensive variation in the response of wild great tit fledglings
to a stuffed sparrowhawk, some showing weak mobbing while others silently
inspected the stuffed raptor closely and resumed begging soon after. This
description of vague anti-predator behaviour in newly fledged wild great tits
further indicates that our results are not an effect of hand rearing or the
absence of parents during maturation in the nest.
Our results show that newly fledged great tits do not have the ability to
recognise a predator. These findings might be an important explanation for
the observations showing that great tits and coal tits experience high
mortality, especially during the first 4 d outside the nest (Perrins & Geer
1980; Naef-Daenzer et al. 1999). In contrast to the absence of predator-
recognition in very young fledglings shown in this study, it seems evident that
ceasing begging when hearing an aerial alarm call (‘seet call’) is innate in
great tit nestlings and develops independently of previous exposure to the call
(Rydén 1978). In addition, in many bird species parents are more likely to
emit alarm calls when their young fledge than at other periods during
breeding (Klump & Shalter 1984 and references therein). Thus, according to
our results, fledglings will most probably not recognize a predator the first
time they see it and we suggest that the presence of parents emitting alarm
calls is of importance to reduce predation risk in newly fledged juveniles.
Furthermore, to experience parents emitting alarm calls in the presence of a
predator most probably enhances an anti-predator response both through
cultural transmission but maybe also by stimulating an early expression of an
innate anti-predator behaviour.
440 C. Kullberg & J. Lind

Acknowledgements
We thank Eberhard Curio, Felicity Huntingford, Sven Jakobsson and Kate Lessells for valuable
comments on the manuscript and Anders Bylin, Sven Jakobsson and Birgitta Tullberg for practical
advice. We are very grateful to Helena Elofsson for taking good care of our birds and to Birgitta
Tullberg for financial support. We also thank the Swedish Ornithological Society (Elis Wides
Foundation to J. L) and Stockholm University (Alice and Lars Siléns Foundation to J. L).

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Received: October 15, 2000

Initial acceptance: April 5, 2001

Final acceptance: November 8, 2001 (M. Taborsky)